Fleas are small parasitic insects that are active exclusively in the adult stage. From the taxonomic point of view, fleas belong to the Phylum Arthropoda, to the Class Insecta and to the Order Siphonaptera, which includes 15 recognized families and about 2500 species. Many of these are ectoparasites of mammals, while only a small percentage parasitizes birds. Fleas of medical-veterinary interest, being ectoparasites of pets and humans, belong to the Family Pulicidae, Subfamily Pulicinae.
The most important species in terms of epidemiology and health, and the species that most frequently infest pets (and humans) are Ctenocephalides felis felis (Fig. 1), Ctenocephalides canis (Fig. 2) and Pulex irritans (Fig. 3). These three species are very similar one with the other, despite their different morphological, biological and ecological characteristics. The spread of fleas in general, and of these three species in particular, is conditioned by the widespread presence of their potential hosts, and thus by the availability of ideal habitats for their development. It has been amply demonstrated that at our latitudes the most popular species is C. felis felis (70% of the flea population), followed by C. canis (25-30%); the spread of P. irritans is instead very limited. Fleas have a strong host-specificity. In fact, C. felis felis recognizes dogs and cats as their main hosts, but can also infest humans, rodents, foxes, mustelids, and occasionally calves, foals, lambs and young goats. On the contrary, C. canis infests a smaller number of animal species: in addition to dogs, cats and humans, it parasitizes rabbits, mice and foxes. The flea species considered typical of humans, P. irritans, also infests foxes, pigs, sheep and, sporadically, dogs and cats.
MORPHOLOGY
In the adult stage, fleas are small brown-black insects (approx. 1-5 mm in length, with males being generally smaller than females). They are wingless and have distinctive features, such as a latero-laterally flattened body, a thick shiny exoskeleton and well-developed limb muscles. These anatomical features make fleas suitable for parasitism. Being insects, the body of the adult flea is divided into three segments: the head, thorax and abdomen. The head of the flea, depending on the species, is elongated anteriorly (Fig. 4) or rounded (Figs. 5, 6); these aspects are diagnostic traits used for the identification of the species present. In addition, some species have morphological characteristics equally useful for their identification, such as cuticular comb-shaped formations, the ctenidia, which can be either genal orpronotal, depending on their anatomical location. These combs are formed by rows of dark spines, located ventrally at the level of the head (genal ctenidium) and posteriorly on the first thoracic segment (pronotal ctenidium). The genus Ctenocephalides has ctenidia (Figs. 4, 5) while the genus Pulex (Fig. 6) has none.
The buccal apparatus, the function of which is to bite the skin and suck the blood, consists of an upper azygos labium located in a median position, an epipharynx traversed ventrally by a deep groove, and a maxillary palpus or lacinia, provided with tiny teeth which the flea uses to pierce the skin of the host.
The thorax is very short and consists of three segments: the prothorax, mesothorax and metathorax, jointed to each other. The thorax has bristles, crests of spines, combs and tiny teeth, oriented antero-posteriorly and dorso-ventrally, thus allowing the flea to remain attached when the animal reacts or attempts to scratch. The thorax has three pairs of limbs inserted in each segment and consists of a coxa, a small trochanter, the femur, tibia and tarsus. The tarsus has two strong sturdy claws that allow the flea to hook onto the host and make space for itself in the animal's fur. The last pair of limbs have well-developed muscles and are suited for jumping. These remarkably developed muscles give fleas their well-known ability to jump, also supported by a large energy reserve provided by a highly specialized protein called resilin. For example, C. felis felis (Fig. 1 [3]) is able to jump about 33 cm high covering a distance of 50 cm. The immature stages (see below) are egg, larva and pupa. The eggs (Fig. 7) have a pearly colour, a smooth surface and are about 0.3-0.5 mm in size, whereas the larvae, apodal, have a yellowish, vermiform body a few mm long and covered with setae. The head is dark-coloured and is provided with a masticating buccal apparatus. At the end of its development the larva turns into a pupa, which is similar to a cocoon a few millimetres in size, in which the adult develops.
BIOLOGY AND EPIDEMIOLOGY
Fleas have a life cycle of complete metamorphosis (holometabolous insects), which consists of four stages of development: egg, larva, pupa and adult.
Only adult fleas have a parasitic activity, while in the immature stages they live in the external environment, outside the vertebrate host (this period of time comprises over 90% of the insect's life cycle). Adult fleas which infest the animal are defined as permanent ectoparasites, as they never voluntarily leave the host.
Mating between males and females occurs in the absence of an active search, since the fortuitous contact between the two sexes releases a pheromone that is perceived by certain receptors on the palps of the male and favours mating. Fleas usually mate after the blood meal, which is essential for the development of eggs and continuation of the life cycle. After being fertilized, the female flea starts producing eggs; the females of C. felis felis start to lay eggs 24-48 hours after the meal, producing a few dozen eggs a day and up to about 2000 eggs during their lifetime. The eggs laid on the body of the animal do not remain attached to the coat of the dog or cat but they fall in the external environment, especially in places where the animal sleeps or spends most of its time.
The eggs fall from the infested coat of the animal mixed with flea faeces, which are spherical droppings in males and spiral-shaped droppings in females, and spread in the environment, where the temperature, humidity and food sources determine the continuation of the biological cycle.
The faeces of fleas, especially the droppings produced by females, are particularly important for larval development. In fact, fertilized fleas ingest much more blood than the amount needed for themselves and for the production of eggs. This large amount of blood is eliminated undigested by the flea and is used by the larvae as nourishment, thus ensuring the survival of future generations. In general, the temperature (~ 20-25°C) and humidity (~ 70-80%) of domestic environments are ideal for the development of fleas; in these conditions the cycle is completed in 2 weeks, but may last up to 3-4 weeks (average 21 days). In unfavourable conditions, the entire cycle can take 6-12 months.
About 48 hours after the laying of the egg, the larva emerges from the egg using a structure called the "egg tooth". The larvae have a positive geotaxis and negative phototaxis, so they tend to hide from direct light. If the eggs are hatched where the infested dog or cat sleeps, i.e. on pillows or armchairs, the larvae tend to hide among the fibres of these objects. The larvae can also settle in fitted carpets, in cracks in the floor of the house or dog house, between the fibres of beds, camp beds, carpets, sofas, where they find ideal environmental conditions (relatively high humidity and temperature between 13°C and 35°C) for their survival and their development. In about a week or so, they undergo two moults and become third stage larvae. In this period the larvae are not very mobile, and they move around by crawling a few tens of centimetres from the point of hatching.
Upon maturation, the third larval stage turns into a pupa through a complex process which consists of emptying the intestine, curving the body into a “U” shape and forming a sticky silk cocoon swaddled by the debris originating from the surrounding environment (e.g., fibres, fragments of hair and skin, dust). The immature adult stage, called pharate, develops inside the pupa. Adult fleas begin to emerge from the puparium about two weeks after the eggs are laid, usually as a result of mechanical stimuli consisting mainly of treading on the floor, pressure on the cocoons and direct contact when the animal walks or lies down. It is important to point out that the immature adult is able to remain inside the cocoon, alive and vital, for many months before continuing its development in suitable environmental conditions and in a host to parasitize. After hatching of the egg, the insect begins to search for a host to jump onto and feed on, helped by specific receptors on its body which perceive various types of stimuli: visual, tactile (e.g., vibrations), chemical (e.g., presence of carbon dioxide) and heat. The pupae of C. canis are able to remain quiescent for long periods (up to one year or more) but, in the presence of a susceptible host, the adult stage can emerge in less than one minute and jump on the host.
After hatching from the puparium, the flea has to intercept and parasitize the host within about 36-48 hours or so; beyond this time limit, it dies of dehydration or depletion of its energy sources.
Although the home environment generally promotes the development of the immature stages and allows the pharate adult stage to remain quiescent in the cocoon until the appearance of favourable conditions, it can also adversely affect the vitality of adult fleas, as they survive better in cooler and more humid environments than those of domestic dwellings. Fleas can also survive in very cold conditions (over 10 days at 3°C but not longer than 5 days at 1°C).
Fleas can be found on animals throughout the year, but the infestation peaks are observed in late spring and early autumn, when the environmental conditions permit and favour larval development. The main source of infestation for animals (and humans) are fleas just hatched from the puparium into the environment, and not from direct contact with infested hosts. At the same time, it is important to emphasize that also open spaces are not a frequent source of infestation, as areas exposed to sunlight (e.g. gardens and lawns) do not offer opportunities for development and survival of the parasite. However, in outdoor environments, places that could allow the development of fleas are generally those shaded from sunlight, such as dog houses, flower beds, and areas under bushes and shrubs.
PATHOGENIC ROLE
The pathogenic role of fleas is tied exclusively to their haematophagy. Adults, males and females, feed on blood, sucking it directly from the blood vessels (blood feeding arthropods) of the host, after piercing the skin with the tiny teeth of the maxillary laciniae. After inserting the hypopharynx into the capillary, the insect sucks the blood made incoagulable by the saliva, which also contains a substance that facilitates penetration of the buccal apparatus. The flea feeds daily or every other day (the male takes less blood than the female) and sucks continuously for about half an hour, at intervals of 5-10 minutes until the next meal; it remains on the body of the animal body for up to two months.
The sucking of blood is the basis of a multifactorial pathological process, related both to direct damages, such as 1) the removal of blood; 2) skin lesions; 3) allergic reactions and hypersensitivity, and to indirect damages, consisting in the possibility of transmitting pathogenic agents.
The deprivation of blood might seem slight (a single flea takes about 14-15 ml of blood per day), if correlated to the individual parasite and its small size. However, in reality the continuous and repeated feeding, especially in cases of massive infestations, may cause iron-deficiency anaemia, especially in young animals.
The most important consequence of the bite is the occurrence of allergic reactions resulting from the contact with certain substances in the saliva of the insect. In general, the first bite inflicted on an animal does not cause noticeable skin reactions; however, when repeated, they can cause intense allergic processes characterized by itching, alopecia, papules and erythema. The lesion is exudative and the drying of the exudate leads to the formation of crusts on the skin of the animal; moreover, since the infested subjects react by biting and scratching in the parasitized regions, the lesions may become worse. In temperate areas, the allergic symptoms resulting from flea bites occur mostly during the summer, when arthropod activity peaks. However, in home environments, as a result of heating, exposure to bites is possible every month of the year and therefore the symptoms may be constantly present.
In a certain percentage of infested subjects, successive bites cause a pathology of considerable veterinary importance, called "flea allergy dermatitis" (FAD). FAD is the result of a type I, caused by the rapid mast cell degranulation (within about half an hour), and type IV (cell-mediated) hypersensitivity reaction, with the intervention of sensitized lymphocytes 1-2 days later. The severity of the clinical picture is correlated to the degree of hypersensitivity of the dog or cat to fleas. In the dog, FAD usually presents with a pruriginous dermatitis with inverted “V”-shaped lesions on the lumbosacral area and characterized by different degrees of alopecia, erythema, papules, crusts and scales. The intense itching leads the animal to violently scratch the region, sometimes causing self-inflicted lesions. The lesions are usually aggravated by a bacterial folliculitis and, if they become chronic, they may evolve into hyperpigmentation and lichenification. In the cat, FAD presents as a nodular, miliary dermatitis, with symmetrical lesions at the level of the back, hips, loins, and occasionally the neck.
As mentioned, fleas can also bite humans, usually in the lower limbs. In humans, flea bites are itchy and lead to the formation of a dark macula surrounded by a rosaceous wheal for days.
Fleas also act as vectors of various pathogenic agents for both humans and animals. For example, C. felis felis and C. canis are intermediate hosts of Dipylidium caninum, a cestode that in the adult stage lives in the intestines of dogs and cats and can also parasitize humans. The final hosts are infested by ingesting the fleas, or residues of them, which may contain up to several dozens of larval pests of the cestode (cysticercoids). Another helminth that identifies the flea as an intermediate host is Dipetalonema reconditum, a filaroid nematode that lives in the subcutaneous and perirenal tissue of the dog. This is not the cause of significant damage, but can be a major diagnostic enigma in microfilariemic subjects.
Fleas can carry bacteria which can be the cause of severe human pathologies, such as Bartonella henselae, Rickettsia conorii and Rickettsia-like agents, transmitted by Ctenocephalides spp., or Yersinia pestis (bubonic plague agent), which is transmitted by the bite of rat fleas.
DIAGNOSIS
The fleas present on the body of an infested animal are easy to find (and to remove), by careful combing with a fine-tooth comb. In case of suspected infestation, without the identification of adult fleas, insect eggs and faeces can be collected from the fur of the animal by brushing the animal and allowing the debris to drop on a moistened paper towel: in cases of infestation, the faeces, containing the undigested blood of the animal, dissolve, staining the paper with intense red areas. Alternatively, if when combing the animal the skin debris and fur fall onto a white surface that is not moistened, the faeces of the insects are easily recognizable as they appear as blackish-brown dots.
Since infested cats lick themselves persistently, they ingest numerous specimens of fleas from their fur, and this can significantly lower the chances of detecting insects on them. In these cases, the oral cavity of the cat can be inspected in order to find fragments of fleas between the teeth or on the spinous processes present on the tongue.
CONTROL AND TREATMENT
In light of the particular life cycle of fleas, which takes place mostly off the host, control of the parasitosis requires an integrated pest management approach, aiming at treating not only the animal but also the environment in which the dog or cat lives.
The home environment should be disinfested using powerful vacuum cleaners on all surfaces that have come into contact with the animal and in any case wherever possible (e.g., animal transport cages, carpets, bedding, pet beds, pillows), paying particular attention to the cracks and fissures which might be present on the floor. Steam cleaners can greatly help the use of a vacuum cleaner, especially if insecticides are added in the steam cleaner boiler. Afterward, insecticide sprays can be used 2-3 times a week every 2 weeks for 2-3 months. The textile surfaces on which pets rest should be cleaned with high temperatures or, if possible, eliminated altogether.
Flea treatment on animals can consist in the use of various classes of molecules, available in different formulations, which have overcome the limitations of the now obsolete organophosphates. Following are some examples of molecules used in the control and treatment of flea infestations.
Pyrethroids have a rapid killing effect and are often combined with certain synergizing compounds (e.g. piperonyl butoxide) to prolong their residual effect. These molecules, such as deltamethrin and permethrin, have an ectoparasiticide and repellent action, which is also exploited in the control of other ectoparasites, such as mosquitoes and sandflies. As an example, permethrin is a molecule that acts on the sodium channels of the arthropod cell membrane, thereby causinghyperarousal of the nervous system and death. In the cat, due to the deficiency of the enzyme glucuronosyltransferase, pyrethroids should not be used, and nor should cats come into contact with recently treated dogs.
Among the chloronicotinyl nitroguanidines, imidacloprid is a relatively new insecticide, which has a neurotoxic action (it competes with the acetylcholine of the parasite) and a long duration of action. This molecule is ingested by the flea with the blood meal, or it can also be absorbed by contact with the cuticle of the exoskeleton of the arthropod.
Among the neonicotinoids, nitenpyram acts on the nicotinic receptor of the acetylcholine of the insects, and can rapidly reduce the flea population.
Other usable molecules are phenylpyrazoles, which have a fairly good killing and residual action, and last up to 3 months. Among these, fipronil acts on the chlorine channels of the nervous system of the arthropod, thereby causing death by hyperarousal of the nervous system. Pyriprole is another phenylpyrazole that acts by rapid contact, killing the fleas within 12-24hours.
Development inhibitors and growth regulators can interfere with the development of flea eggs and larvae. For example, lufenuron, when ingested by fleas, passes into the eggs and blocks the formation of chitin, thereby preventing the development of larvae. On the contrary, methoprene acts as an analogue of a juvenile insect hormone, and by stimulating the production of a high level of this hormone it inhibits larval metamorphosis and moults from larva to pupa.
Recently, a new insecticide molecule has been produced, metaflumizone. It belongs to the group of semicarbazone derivatives, which cause voltage-dependent blockage of the sodium channel of the insects, resulting in progressive paralysis starting from the buccal apparatus of the flea. Metaflumizone is available for the control of feline pulicosis and is also used in combination with amitraz for the simultaneous control of flea and tick infestations in dogs.
In fact, there are also combinations of the different molecules. For example, a spot-on combination containing permethrin and imidacloprid is available on the market. It has a neurotoxic synergistic adulticidal (killing for about 4 weeks the fleas which are already present and those that can re-infest the dog) and larvicidal (killing the larvae present in the environment by contact with and feeding of the skin debris eliminated by the treated dog) effect. Another combination, containing fipronil and methoprene, combines both the insecticidal action of the first molecule and the inhibiting action on development of the immature stages of the growth regulator.
Suggested readings
- 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. 1999. L’infestazione da pulci nei carnivori domestici. Obiettivi e Documenti Veterinari Supplemento n.4, pp. 49-55.
- 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. 710-719.
- Otranto D., Dantas-Torres F. 2010. Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasites and Vectors, 3: 2.