babesiosis

Pictures

Picture	Title	Caption	Copyright
Title Histology Caption Babesiosis: B. bigemina in erythrocytes. Copyright ©USDA-2002/Foreign Animal Diseases Training Set/USDA-Animal and Plant Health Inspection Service (APHIS)	Histology	Babesiosis: B. bigemina in erythrocytes.	©USDA-2002/Foreign Animal Diseases Training Set/USDA-Animal and Plant Health Inspection Service (APHIS)
Title Histology Caption Babesiosis: B. bovis in erythrocytes. Copyright ©USDA-2002/Foreign Animal Diseases Training Set/USDA-Animal and Plant Health Inspection Service (APHIS)	Histology	Babesiosis: B. bovis in erythrocytes.	©USDA-2002/Foreign Animal Diseases Training Set/USDA-Animal and Plant Health Inspection Service (APHIS)
Title Histology Caption Babesiosis: B. caballi in erythrocytes. Copyright ©USDA-2002/Foreign Animal Diseases Training Set/USDA-Animal and Plant Health Inspection Service (APHIS)	Histology	Babesiosis: B. caballi in erythrocytes.	©USDA-2002/Foreign Animal Diseases Training Set/USDA-Animal and Plant Health Inspection Service (APHIS)
Title Histology Caption Babesiosis: B. equi in erythrocytes. Copyright ©USDA-2002/Foreign Animal Diseases Training Set/USDA-Animal and Plant Health Inspection Service (APHIS)	Histology	Babesiosis: B. equi in erythrocytes.	©USDA-2002/Foreign Animal Diseases Training Set/USDA-Animal and Plant Health Inspection Service (APHIS)

Identity

Preferred Scientific Name

• babesiosis

International Common Names

• English: babesiosis, babesia, in food animals- exotic; malignant jaundice; piroplasmosis; red water; texas fever; tick fever
• Spanish: fiebre del Texas; la tristeza
• French: piroplasmose bovine

Overview

The parasite Babesia is named after Babes, the scientist who first described it in sheep and cattle in 1888 (Levine, 1961). Organisms belonging to the genus Babesia are pear-shaped and parasitize red blood cells of mammals and invade the internal organs of ticks (Nyindo, 1992). In ticks, Babesia parasites may be transmitted trans-stadially (from larva to nymph to adult) and transovarially (Friedhoff and Soule, 1996). Although typically pyriform, they may be circular, oval or amoeboid with lateral chromatin in one or more nuclei (Morel, 1989).

Babesia belongs to the family Babesiidae (Poche, 1913). Organisms of the family Babesiidae are round to pyriform or amoeboid forms occurring in the erythrocytes. They multiply by binary fission or schizogony, in the red blood cells. The vectors are ixodid ticks (Soulsby, 1986). Babesia belongs to the order Piroplasmidia Wenyon,1926. Members of this order are blood parasites of vertebrates, and they are small, round or pleomorphic. Their apical complex is reduced and reproduction is by binary fission or schizogony. They are parasites of the haematopoetic system with ticks as their vectors (Soulsby, 1986). Babesia belong to the class Sporozoea Leuckart, 1879. Members of the class Sporozoea are parasitic and produce spores. They possess no organs of locomotion, such as cilia or flagella, except in the gamete stage. Reproduction is asexual by binary or multiple fission (schizogony) or sexual (gametogony). Gametogony leads to the formation of a zygote which in turn initiates the process of sporogony or spore formation (Soulsby, 1986).

Over 100 species of the genus Babesia have been described (Homer et al., 2000) and a large number occur in domesticated animals (Nyindo, 1992). Clinical cases are described as babesiosis whereas sub-clinical infections found in young animals and those recovered from clinical attack are termed babesiasis (Nyindo, 1992). On the basis of host and Babesia species involved, babesiosis may be termed bovine babesiosis, canine babesiosis, ovine babesiosis, equine babesiosis, porcine babesiosis (Morel, 1989; Nyindo, 1992). The Babesias affecting cattle are usually conveniently divided into two groups, large (Babesia bigemina and B. major) and small (Babesia divergens and B. bovis). The Babesias of dogs and wild canidae can also be described as large (B.canis) and small (B. gibsoni). Similarly, the Babesias of equines are either large (Babesia caballi) or small (Babesiaequi) and porcine Babesias also as large (Babesia trautmanni) or small (B. perroncitoi).

In sheep and goats, large (Babesia motasi) and small (Babesia ovis) Babesias may occur (Nyindo, 1992). Babesia felis occurs in cats whereas B.microti occurs in rodents. In the reindeer, Babesiajakimovi clinical infection is likely (Nyindo, 1992). In the past, speciation was mainly based on morphology of the parasite and the host affected. Today species are identified on the basis of molecular and antigenic data, host specificity and pathogenicity. Morphology is of relatively minor importance as it may be affected by the host species (Zintl et al., 2003).

Babesiosis is a composite term for diseases caused by parasites of the genus Babesia. The disease affects both domestic and wild mammals. Mammal species belonging to the same or related genera, are usually receptive to the same Babesia species. Thus Babesia bigemina and B. bovis can infect taurines, zebu, and African and Asian buffalo; B.motasi, B. ovis and B. crassa infect sheep, goats and all wild species or sub-species of the sub-family Ovinae; B caballi and B. equi infect horses, donkeys and zebra. Dogs, various wolves and jackals are receptive to B. canis and B. gibsoni (Morel, 1989). In endemic areas, the disease can causes serious economic losses to the livestock industry. Although infections with some of the less pathogenic bovine and ovine spp (such as, B. divergens, B. bigeminaB. motasi and B. crassa) are often associated with mild clinical signs and may be missed by the farmer or clinician (Atkas et al., 2005; Morel, 1989; Zintl et al., 2005), acute clinical babesiosis in cattle or sheep has a grave prognosis and may be fatal without treatment (30% for B.bigemina, 70-80% for B. bovis, 30-50% in B. ovis). Equine babesiosis has a mortality rate of 20-50% but can occur in acute, sub-acute or chronic forms (Friedhoff and Soulé, 1996). Similarly, clinical signs of canine babesiosis can range from subclinical to a hyperacute fulminating fatal disease similar to complicated malarial infections (Boozer and Macintire, 2003). Babesiosis in pigs is generally mild, although infections may be aggravated by concurrent infections or poor nutrition (Waal et al., 1992).

In general, the disease is less serious in the traditional management system in endemic areas where tick control is loose. This is thought to be due to a phenomenon known as enzootic stability. In such situations young animals are exposed to the parasites even before the disappearance of passive protection by colostral antibodies. Calves and foals are protected for up to a year by an additional mechanism, known as inverse age resistance, which is independent of the immune status of the mother (Christensson, 1987; Waal and Heerden, 1994). In these animals low levels of parasitaemia may persist for a long time without any apparent ill-effects. Thus, in areas with high infection pressure most animals acquire immunity without showing clinical signs. In modern management systems tick control can destroy the state of enzootic stability by making the vector scarce (after treatment) and thereby increasing the risk of clinical disease (Morel, 1989). Very high losses may also be sustained when groups of susceptible adult animals are moved into areas of endemic babesiosis (Adam et al., 1978).

The taxonomic position of B. equi among the Babesia spp. has been questioned for some time because it has a pre-erythrocytic stage in its life cycle (see below) similar to Theileria spp. Comparisons of the 18s rRNA gene sequence confirm its close relationship to Theileria (Homer et al., 2000; Friedhoff and Soulé, 1996). Similarly, B. microti, a rodent parasite and important pathogen of humans, is thought to be more closely related to Theileria than the other Babesia spp. (Homer et al., 2000).

Hosts/Species Affected

Mammal species usually belonging to the same or related genera are receptive to the same Babesia species. Thus B. bigemina and B. bovis can infect taurines, zebu, African and Asian buffalo; B. motasi and B. ovis infect sheep and goats, and all wild species or sub-species of the subfamily Ovinae; B. caballi and B. equi infect horses, donkeys and zebras; whereas dogs, various wolves and jackals are receptive to B. canis and B. gibsoni (Smith et al., 1972; Morel, 1989).

Amongst cattle, there is some evidence of a difference in breed susceptibility to infection. Zebu, for example, are less susceptible to Babesia than taurines; the disease is less serious and with fewer relapses. Bos indicus cattle and their crosses are more resistant to babesiosis and adverse environmental conditions than breeds imported from Europe. For example, Droughtmaster cattle carry ten times fewer ticks than cattle of the British breeds (Francis, 1966; Losos, 1986) and Sahiwal cattle possess higher innate resistance to B. bigemina than Charolais cattle (Lohr, 1973).

Sheep and goats are equally receptive to Babesia, but, depending on the parasite species or strain of a given species, goats are usually less susceptible and may only have a latent infection.

Generally, in Africa the traditional, local breeds are hardier and less susceptible to Babesia, because they are better adapted to the local climatic and feeding conditions. Another reason is their genetic diversity due to the large number of allelomorphic genes. Breeds developed for higher productivity, with special climatic or feeding requirements, are susceptible because of their poor adaptability due to the limited number of alleles present (Morel, 1989).

In terms of age there is an inverse age resistance to Babesia infection in that the young are less susceptible to babesiosis than older animals (Urquhartet al., 1996). Compared with most other infectious diseases, which affect juveniles more severely than adult animals, inverse age resistance is unusual. This phenomenon is evident only in cattle and horses and persists longer than passively transferred antibodies (Goff et al., 2003; L’Hostis et al., 1995; Smith et al., 2000; Waal and Heerden, 1994). It is thought to be due to innate resistance and independent of the maternal immune status (Christensson, 1987). In contrast, puppies, kids and lambs that are unprotected by maternal antibody are more severely affected by Babesia than adult animals (Bai et al., 2002; Martinod et al., 1986; Yeruham et al., 1998). Another factor that appears to ensure non-specific protection against Babesia is the presence of the spleen. Splenectomized calves become fully susceptible to infection (Edelhofer et al., 1998) and unnatural hosts that are normally fully resistant to Babesia may have severe infections if the spleen is removed. The most notable example for this are zoonotic B. divergens infections in splenectomized humans (Gorenflot et al., 1998).

The animal’s physiological condition also influences the natural or acquired defence mechanism. Any loss of condition due to fatigue, nutritional problems and/or anabolic deviation (lactation, fattening, gestation) increases an animal’s susceptibility to a primary infection or a relapse (Morel, 1989; Urquhart et al., 1996). Diseases (chills, infectious diseases, vaccinations etc.) have the same effect. Relapses due to cold are very common in babesiosis, as are those due to abrupt weather changes that disturb physiological controls (Sirocco in northwestern Africa). Cases of winter babesiosis are common in temperate zones, and during the cold season in tropical zones, although the vectors are not active in that season (Morel, 1989).

The type of animal husbandry also influences establishment of babesiosis. For instance, porcine babesiosis occurrence is determined by contact of domestic pigs with wild suids (in partially free-range herds) or their ticks (chance of introduction into a piggery). The role of wild boars, warthogs and river hogs as Babesia reservoirs, and their proximity and possible contacts with domestic pigs can explain the sporadic nature of porcine babesiosis in herds.

In endemic areas, where there are many infected ticks, the immunity of the host is maintained at a high level through repeated challenge and overt disease is rare. In contrast, where there are few ticks or when they are confined to limited areas, a portion of young animals fail to become infected while still protected by maternal antibody and/or other innate mechanisms and retain their susceptibility.If in these circumstances, such as in intensive systems of husbandry, the numbers of ticks suddenly increases due to favourable climatic conditions or to a reduction in dipping frequency, the incidence of clinical cases may rise sharply (Urquhart et al., 1996). In tick-vector-free areas, animals kept under intensive systems of management do not acquire the infection but such cattle are very susceptible when introduced into endemic areas with high infection pressure and in such cases losses are heavy (Losos, 1986).

Tick vector infestation is generally higher among extensively managed (nomadic) cattle than those maintained under semi-intensive or intensive management (Biu, 1997). The difference may be due to the improved management and general veterinary attention to the animals under semi-intensive or intensive condition of management.

Several factors, such as latitude, altitude and their effects (sunlight, temperature, rainfall, wind pattern) influence the distribution of the vector of babesiosis (Morel, 1989). In regions with uniform climatic conditions such as West Africa, a comparison of data on tick species distribution with isotherm and isohyet maps enable the identification of natural distribution zones in relation to latitude. In mountainous regions, the determining factor is altitude. According to its micro or mesoclimatic requirements, the tick species will be found in certain similar bioclimatic zones, and not in others. Moreover, seasonal variations within a bioclimatic zone will favour or hinder the development or activity of a tick during certain periods (Morel, 1989; Rabo et al., 1995). In tropical climates the dominant factor is rainfall (Morel, 1989). Tick infestation has been shown to be higher during the rainy season than the dry season in southwestern Nigeria (Dipeolu, 1975) and in northern Nigeria (Rabo et al., 1995). Outbreaks of babesiosis during such periods of heavy tick infestation have been reported (Rabo et al., 1995). In northern hemisphere temperate climates disease distribution typically has a bimodal seasonal distribution with a spring peak between April and June and an autumn peak from August to October. Once the threshold temperature for tick activity has been exceeded, the chief determining factor for tick infestation is humidity (Gray, 1980).

Distribution

A variety of Babesia species parasitize erythrocytes of domestic animals causing fever, anaemia, jaundice and haemoglobinuria. The parasites were thought to exhibit strict host specificity but this concept has now been outdated (Nyindo, 1992).

The following Babesia species cause disease in mammalian hosts found in the various locations where relevant tick vectors occur (Table 1).

Table 1: Geographical distribution of Babesia parasite, the hosts and tick vectors involved

Source: Smith et al. (1972), Morel (1989), Kakoma and Mehlhorn (1994) and Hong et al. (1997).

During 2011, Babesiosis was reported to the AU-IBAR by 15 countries who recorded a total of 1,012 outbreaks, 37,525 cases and 271 deaths (AU-IBAR, 2011). Egypt recorded the highest number of outbreaks (601) followed by Zimbabwe (219), and Swaziland (50). The corresponding number of cases was highest in Egypt (29,624), followed by Tanzania (6,521) and Zimbabwe (478).

Countries reporting babesiosis to AU-IBAR in 2011

NS=Not specified

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Pathology

The gross postmortem and microscopic lesions of bovine, ovine, equine and porcine babesiosis have been reviewed (Morel, 1989). In haemolytic babesiosis, icterus is seen upon opening the carcass, by the colour it gives to all the connective tissues, and internal and external mucosae. The bladder contains haemoglobinuric urine. Splenomegaly is invariably present, with a dark red, mushy pulp due to degeneration of the haematopoietic centres. Prominent Malpighian corpuscles, due to hyperplasia of the reticular tissue, are observed in the middle of this pulp. The liver is enlarged and congested, with discoloured patches on a brownish background. On section, the lobule is seen to have a yellow centre with a grey border. The bile is granular. In hypertrophic kidney the two zones, cortical and medullary, are not clearly distinguishable. In the case of pneumonia due to icterus, the lungs show hepatization and local congestion, with rust-red mucus, and sometimes small haemorrhages. Petechia may be present on the peritoneal and cardiac serosae. If icterus is slight, the muscles appear pale because of anaemia and fever.

In the case of babesiosis due to B. bovis with nervous signs, there are petechia and congestion spots in the cerebral cortex. Ecchymosis and petechia are observed on the epicardium, in the myocardium, on the kidney, and in the renal parenchyma. Microscopically, the hepatic parenchyma presents centrolobular necroses and hydropic vesicular degenerating patches. Many macrophages contain red blood cell with or without parasites. The kupffer cells contain hemosiderin deposit in the tubular epithelium and reticulum cells of the glomeruli. The main tubular epithelium degenerates in the nephrons. Other microscopic lesions of babesiosis due to B. bovis include microthrombi that dilate the cerebral cortical capillaries. They are composed of a mass of parasitized erythrocytes, with peripheral interstitial oedema. The same microthrombi from agglutinated parasitized erythrocytes are found in the interlobular capillaries of the kidneys, causing congestion and petechia.

In principle, the ovine and porcine babesiosis lesions are the same as those of bovine babesiosis. In pigs, congestion, petechia and oedema are more common and pronounced.

Although the lesions of equine babesiosis are not very different from bovine babesiosis, those of equines show some peculiarities. These include haemorrhage on the external and internal mucosae, hypertrophy and inflammation of the lymph nodes, and abundant exudates in the pericardium and peritoneum. The pathology of canine and feline babesiosis has been reviewed (Nyindo, 1992). The mucous membrane becomes pale but jaundice and haemoglobinuria are uncommon. The spleen increases in size, and ascites, oedema of subcutaneous tissue, keratitis and iritis may be observed. Dogs that die of chronic babesiosis are emaciated. The subcutaneous tissue, fascia, fat and mucous membranes are stained yellow. The spleen and liver are enlarged. Peritoneal, pleural and pericardial cavities are full of serous fluid. Lungs are oedematous and there is broncho-pneumonia. The heart may be distended but in most cases no striking lesions are seen. The food contents in the gastro-intestinal tract are coloured yellow. Kidney shows evidence of nephrosis and nephritis. The pathology of feline babesiosis is mainly that of icterus and anaemia (Urquhart et al., 1996).

Diagnosis

Clinical Diagnosis

Clinical manifestations of babesiosis are so capriciously variable that they are of little help in diagnosis. The signs common to most cases include fever, malaise and listlessness, anorexia and anaemia. Icterus, haemoglobinuria and ascites may appear during late stages and progressive debility terminates in death (Smith et al., 1972). Breathing is laboured and rapid and the heartbeat is fast and loud. Nervous signs are characterized by hyperexcitability and the animal may charge moving objects. The vision becomes impaired. Urine may have a red-tinged colour (because of haemoglobinuria), hence the name 'red water' (Nyindo, 1992). In milking cows there is a fall in yield. Other manifestations include salivation, lachrymation, diarrhoea or constipation, delirium and incoordination of gait (Hall, 1977). In ruminants, ruminal movement ceases and abortion may occur (Urquhart et al., 1996). In canine babesiosis the disease may be peracute and haemoglobinuria and jaundice are not common manifestations. Similarly, haemaglobinuria is not a common finding in equine babesiosis and jaundice does not occur in donkeys (Nyindo, 1992).

Differential Diagnosis

There are a number of diseases and or conditions that could be confused with babesiosis because of the similarity of clinical signs.

The blood-tinged urine may be taken as a tentative diagnosis but other causes leading to the appearance of 'coffee-coloured' urine, like bovine haematuria and tumours of the urogenital system must be considered in differential diagnosis. Presence of tick/s on the carcass may aid in the diagnosis. Nervous signs may also occur in heartwater (cowdriosis) and Nagana (trypanosomiasis) (Nyindo, 1992). Acute haemolytic babesiosis can be confused with leptospirosis. In the latter case, the occular mucosa is dark red, internal mucosae are haemorrhagic, and the general condition is more markedly affected (Morel, 1989). Leptospirosis has a shorter course and is characterized by being more severe in young animals (Hall, 1977).

Chronic babesiosis or long convalescence from babesiosis can be confused with anaplasmosis which is also tick-transmitted and hence occurs at the same time and in the same environment (Morel, 1989). In anaplasmosis the disease is usually less acute than in babesiosis and haemoglobinuria is uncommon (Hall, 1977).

Laboratory Diagnosis

Parasitological diagnosis resolves difficulties of clinical or post-mortem diagnosis and enables interpretation of the serological test results. It justifies a prognosis based on the Babesia species and parasitaemia rate (Morel, 1989). Babesiosis can be confirmed from Giemsa-stained blood smears (Urquhart et al., 1996) or Romanowsky-stained smears (Soulsby, 1986). In cases where clinical examination shows no characteristic signs, the demonstration of Babesia does not support an immediate diagnosis. It is useful to determine whether the case is a mild form of babesiosis or a chronic infection that has resurged following breakdown of immunity during some other disease, which must be identified.

In B. bigemina infection the severity of the disease can be assessed from the percentage of parasitized red blood cells. The babesiosis is mild or a resurgence of a parasitaemia from a different cause, if the parasitaemia rate is up 1%. The infection is subacute but not too serious at a rate of 5-10%, but serious around 50%,. With B. bovis, the presence of parasite indicates a case of bovine tropical babesiosis, with varying degrees of severity, because parasitaemia in the peripheral blood is considerably lower than in the internal organs. In acute tropical babesiosis, impression smears of congested organs show small or punctiform babesial bodies in agglutinated red blood cells (Morel, 1989). The parasitological tests (using Giemsa- or Romanowsky-stained smears) are simple, cheap and more suitable for field use in remote regions and developing countries.

Immunodiagnostic tests (particularly IFAT) are increasingly used to detect infection, especially in the subclinical situation when organisms are not demonstrable in the blood (Soulsby, 1986) or during chronic infection (Morel, 1989).

In practice, there is no completely satisfactory method that can dispense with detection of the parasite. The serodiagnostic tests include complement fixation test, indirect fluorescent antibody test, indirect haemagglutination test, gel diffusion – precipitation test, rapid card agglutination test, capillary tube agglutination test , antigen-latex complex agglutination test (Morel, 1989; Urquhart et al., 1996) and enzyme-linked immunosorbent assay (ELISA) (Goncalves-Ruiz et al., 2001; Boonchit et al., 2006; Loa et al., 2004). The indirect fluorescent antibody test is species specific and remains positive for 2 years [after infection]. Both the complement fixation and the tube agglutination tests are positive in cattle up to 6 months of infection and, therefore, are inferior to the indirect fluorescent antibody test (Nyindo, 1992). The rapid card agglutination is of little use in the field as it detects differences of strains, not species (Morel, 1989), although it is very sensitive. The antigen-latex complex agglutination test gives excellent laboratory results better than those of the complement fixation. In the field, the proportion of false-positive reaction is 12.5%. However, the test is simple and rapid enough for epidemiological evaluation, and allows immediate decisions to be made concerning treatment on a herd scale. The gel diffusion-preparation test has few practical applications and the indirect haemagglutination test requires sophisticated equipment (Morel, 1989). One problem associated with all immunodiagnostic tests is the need for larger amounts of parasite antigens. Although in vitro culture systems have been developed for most if not all species, they are cost-and labour-intensive. Considerable research effort is currently directed at producing recombinant diagnostic antigens (Boonchit et al., 2006).

The most sensitive and specific methods for detection are molecular. The most common method used to detect Babesia in both the tick and the vertebrate host involves simple or multiplex PCR-amplification of the 18SrRNA gene fragment (see Alhassan et al., 2005; Estrada-Pena et al., 2005; Foldvari et al., 2005; Tomassone et al., 2005). Unfortunately, so far PCR cannot be used routinely, because the equipment and reagents are costly and may not be readily affordable particularly in disadvantaged settings.

Immunology

Early workers on babesiosis thought that Babesia species exhibited mammalian host specificity. However, it has now been shown that a Babesia species can infect a variety of animals: baby mice can be infected with B. canis; B. bigemina has been transmitted to horse; and human beings can be infected by B. microti (Nyindo, 1992) and B. divergens (Gorenflot et al., 1998).

Similar to other protozoan blood parasites, Babesias are known to evade host immune responses by antigenic variation. B. bovis, for example, disguises itself by modifications to its primary surface antigen, VESA1 (Dzikowski and Deitsch, 2006). Antigenic variation may result in a lack of immunologic cross-reactivity between different geographical isolates, which may leave imported animals although immune against their own local strain fully susceptible to disease (LeRoith et al., 2005). It is thought that specific opsonic antibodies (IgG2) may be responsible for controlling parasitaemia by stimulating increased phagocytotic activity once the acute infection has been resolved (Brown, 2001; Goff et al., 2002a). For instance immunity can be conferred passively by inoculation with immune serum (Ben Musa and Dawoud, 2004) or administration of colostrums from immune animals (Jenkins, 2001). In contrast, age-related resistance to primary infection appears to be antibody-independent (antibodies appear late in the primary infection and long after parasites have been cleared from the periphery (Guglielmone et al., 1997a)). As mentioned previously, calves and foals, though fully susceptible to infection, are protected from disease by inverse age resistance (Goff et al., 2003; L’Hostis et al., 1995; Smith et al 2000; Waal and Heerden, 1994). This innate resistance to disease lasts for 9 to 12 months and does not occur in puppies, kids or lambs (Bai et al., 2002; Martinod et al., 1986; Yeruham et al., 1998). The mechanisms underlying this phenomenon are poorly understood, but it has been suggested that differences in the localization and timing of the inflammatory response between young and adult animals may at least be partly responsible (Zintl et al., 2005).

The spleen iscrucial in the maintenance of immunity in babesiosis, indicating that cellular mechanisms are also involved Primates, including humans are resistant to B. divergens infections but suffer severe, frequently fatal disease if they have been splenectomized (Zintl et al., 2003). Similarly, splenectomized calves lose their innate resistance to disease (Wright and Kerr, 1977; Davies et al., 1958; Lohr, 1973). Cellular responses against babesiosis are chiefly mediated by type-1 cytokines. Interferon-gamma and tumour necrosis factor alpha, together with parasite antigen activate mononuclear phagocytes/macrophages to release reactive nitrogen and oxygen intermediates (Goff et al., 2003; Goff et al., 2002a,b; Shoda et al., 2000). This attack by the host defence results in the appearance of intracellular crisis forms, which are indicative for the likely recovery of the host. Phagocytosis of infected erythrocytes also occurs (Shoda et al., 2000; Court et al., 2001), but is probably not significant for the resolution of primary infections. Mobilization of the mesenchymal reserves, hyperplasia of the reticuloendothelial system in the bone marrow, lymph nodes, spleen and liver may be central to subsequent attacks.

List of Symptoms/Signs

Disease Course

There are two principal mechanisms by which babesial organisms cause cellular and tissue injury (Kakoma and Mehlhorn, 1994; Urquhart et al., 1996). The first, intravascular haemolysis, is a direct result of erythrocyte rupture caused by rapidly dividing and exiting parasites. The rate of haemolysis is directly proportional to the parasitaemia which may range between 0.01 - 0.2 % (typical for B. bovis) and 40% (e.g. B. bigemina, B. divergens). Depending on the Babesia species and the immune status and age of the host, the disease may be acute, chronic or inapparent. The acute syndrome is characterized by fever, anaemia, haemoglobinuria, jaundice and variable mortality. The chronic syndromes are poorly defined clinically and are associated with anaemia and variable weight loss, while the carrier state is asymptomatic (Losos, 1986). If untreated the acute form may be fatal within a few days, whereas the chronic form lasts several days or weeks (Urquhart et al., 1996). Following recovery from clinical disease, subclinical infections may last for several years. During recovery, the anaemia which was normocyctic at first, becomes macrocytic and leucocytosis due to a rise in the number of lymphocytes occurs. Relapses are associated with the resurgence of the parasitaemia. In field situations where there is repeated exposure to challenge, the incidence of detectable parasitaemia is higher than that found in single infections, fluctuates widely, and gradually decreases over a period of years. In enzootic areas, the incidence and level of patent parasitaemia decline as an animal ages since it is constantly exposed to re-infection by all the antigenic types found in a particular habitat (Losos, 1986). This simple haemolytic anaemia is characteristic of B. bigemina and B. divergens.

In other species such as B. bovis, B. canis and B. caballi, more severe disease signs are caused by the clumping of infected erythrocytes and adherence to capillaries. As a result, blood flow to vital organs is interrupted resulting in anoxia, organ damage and shock. Accumulated parasites cause allergic reactions at the site of concentration and trigger the release of kinins and other vasoactive substances, resulting in vasodilation, circulatory collapse and death. Involvement of the central nervous system is common and manifests itself in hyperexcitability, muscle trembling, teeth grinding, ataxia, paddling of limbs. Coma and death may ensue. This cellular adhesive phenomenon has been linked to ‘stellate protrusions’ formed on the surface of B. bovis-infected erythrocytes similar to the knobs typical of Plasmodium falciparum infections (Cooke et al., 2005). Another effect that has been described is an increase in erythrocyte fragility. This occurs in both B. bigemina and B. bovis infections and affects uninfected as well as infected erythrocytes.

The pathogenesis of B. bovis infection in cattle is summarized here(Nyindo, 1992). The early events consist of activation of Kallikrein system. Later there is a state of haemolytic anaemia and blockade of blood vessels of the central nervous system. Kallikrein is an enzyme which acts on plasma 2-globulins to produce bradykinin. Bradykinin increases vascular permeability, causes vasodilation and coagulation. Complement cascades are also activated. The results of these reactions are circulatory stasis and shock. The anaemia is macrocytic, hypochromic and the animal gets into a state of anoxia and shock. The osmotic fragility of the normal red blood cell increases and may facilitate parasite penetration, or lead to spontaneous lysis. Anaemia may also become more severe due to removal of erythrocytes by macrophages (Morel, 1989; Nyindo, 1992). Antigen and antibody complexes, with complement lodge in the kidneys and cause glomerulonephritis (Nyindo, 1992).

The haematological changes, which accompany the anaemia, include increased levels of serum glutamic oxaloacetic transaminase (SGOT) and serum glutamic pyruvic transaminase (SGPT), alkaline phosphatase, unconjugated billirubin, blood urea nitrogen (BUN) and, in the late stages of infection, a decrease of calcium. The whole blood clotting time, partial thromboplastin time and prothrombin time are prolonged, and the numbers of platelets are reduced. Leucocyte counts fall slightly at first but in the post-acute phase there is two- to three-fold increase over normal values due to lymphocytosis (Losos, 1986).

Epidemiology

As Babesia infections in ticks persist through molts (trans-stadial maintenance) and is transmitted transovarially (Lewis and Young, 1980), the parasite may be maintained in the tick population for several generations even in the absence of infected mammalian hosts (Donnely and Peirce, 1975). Much progress has been made in the elucidation of the life cycles of the different species of Babesia in ticks. The developmental stages are recognized in the tick gut, haemolymph, ovary and salivary glands (Nyindo, 1992).

Riek (1966) provided a detailed account of the different morphological forms of Babesia bigemina developing in the tick Booplulus microplus. Mehlhorn et al. (1980) outlined the development of B. canis in Dermacentor reticulatus. Moltman et al., (1982) described the fine structure of B. ovis in Rhipicephalus bursa. Electron microscopic studies of the developmental forms of B. divergens in the tick gut, haemolymph, ovary and salivary glands have provided detailed information on the life cycle of the parasites in the vector (Mackenstedt et al., 1990).

The developmental forms of B. bovis in the gut, haemolymph, epidermis, muscle, Malphigian tubules, ovary and eggs of the tick R. bursa have been recognized and names such as merozoites, vermicules or spherical bodies have been assigned to them. However, Moltmann et al (1982) argue that since there is evidence for a sexual stage in Babesia the name kinete should be ascribed to all motile forms previously described under the different names.

Light and electron microscopic studies on the developmental stages of B. canis in the gut of D. reticulatus have been made. Examination of the gut contents of ticks after repletion showed that most of the pear-shaped parasites were lysed (Levine, 1988). Only the ovoid forms persisted and appeared to undergo further development. In the erythrocytes of Beagle dogs, parasites contained many vacuoles, double walled organelles and a homogenous nucleus. Some of the ovoid forms developed spiky protrusions, which contained 1 to 5 microtubules (‘ray bodies’). Within 48 hours following repletion red blood cells were digested and the ovoid forms and those with spikes were released. Each form was bounded by a typical membrane. The liberated forms invaded the gut wall of the tick. Two forms have been recognized in the gut cells: those with only one nucleus and those with more than one nucleus.

According to Nyindo (1992), studies involving B. microti and Ixodes dammini demonstrated the presence of parasites each with an arrowhead structure. Microtubules and cytostomes were also seen. The parasites occurred in the gut lumen and in close contact with gut cells or basal lamina. After syngamy parasites entered cells of the gut and transformed into club- or cigar-shaped kinetes. Kinetes of B. ovis, B. bigemina, B. caballi and B. divergens enter the tick haemolymph from where they are disseminated throughout various tissues including the musculature, epidermis, Malpighian tubes and ovaries. Here the kinetes undergo secondary cycles of schizogony to produce more kinetes. Developing eggs may be invaded followed by a secondary cycle of schizogony in gut cells of the transovarially infected embryo.

In contrast, B. microti and B. merionis do not produce progeny kinetes. In these latter species the parasites invade the salivary glands soon after leaving the gut. Developmental stages in the tick salivary glands have been described in a number of species (Schein et al., 1979; Moltman et al., 1982; Mackenstedt et al., 1990).

Usually 24 h following the tick attachment, cigar-shaped kinetes can be recognized in the haemolymph. By 48 h the kinetes are found in the cytoplasm of non-secretory glands where they develop into sporozoites. Sporozoites increase in number by binary fission or by schizogony. After binary fission or schizogony no further development of the sporozoites occurs and at this stage the parasites are not infective to mammalian hosts. Parasite differentiation and acquisition of infectivity is induced while the tick is feeding on the animal or by incubating ticks at 37°C (Nyindo, 1992). Sporozoites are released in the tick saliva and are infective to the respective mammalian hosts when the tick is feeding.

Upon inoculation into a new host, Babesia usually invade erythrocytes directly. The only exception to this rule is B. equi, which invades lymphocytes during a pre-erythrocytic stage (Friedhoff and Soulé, 1996). The process by which Babesia invade red blood cells is poorly understood but appears to involve sialic acid residues on the host cells surface (Gaffar et al., 2003; Okamura et al., 2005; Zintl et al., 2002). After attachment to the host cell and orientation of the apical end towards the erythrocyte surface, secretory products released by the rhoptries cause the erythrocyte membrane to invaginate. At first a parasitophorous vacuole encloses the sporozoite. As the vacuole membrane disintegrates, the parasite is eventually limited by one single plasma membrane, which is directly in contact with the erythrocyte cytoplasm (Gorenflot et al., 1991; Igarashi et al., 1988). Development in the erythrocyte begins with the trophozoite. It is circular, elliptical, small in size, and with a nucleus. It grows in size and the nucleus doubles to form the trophoblast. Budding of the trophoblast gives two or four oval or pyriform organisms, linked by the cellular debris of the trophozoite. The whole represents the schizont. The separate elements are the merozoites, each with one nucleus in the case of a tetrad, or with two nuclei for a pair. Each merozoite continues the infective cycle after destruction of the erythrocyte. The vast majority of merozoites continue to multiply asexually while a small proportion turn into non-dividing spherical gamonts, which remain inside erythrocytes until they are taken up by ticks during feeding (Mackenstedt et al., 1990).

Impact: Economic

Of the more than 70 species of Babesia that infect domestic animals, bovine babesiosis is undoubtedly the most economically important. It is estimated that up to 500 million cattle are infected with Babesia parasites each year, representing a huge economic burden on the beef and dairy industry worldwide (Cooke et al., 2005). Depending on the pathogens involved and the susceptibility of local cattle, economic losses due to tick-borne babesiosis may represent up to 20% of the value of the livestock (Morel, 1989). This assertion, which is general, is dated 1989. In Brazil, annual losses due to Boophilus microplus vector of babesiosis and anaplasmosis, stood at US$ 1 billion as at 1992 (Evans, 1992). Babesiosis was estimated to cost the Australian beef industry $A30 million per year in 1994 (Harper et al., 1994) and possibly 10 million cattle are at risk. A study carried out in Cuba between 1985 and 1995, estimated that the losses arising from morbidity, mortalities and reduced milk production caused by tick-borne diseases and the cost of ascaricide treatment amounted to almost US $7 million per year (Fuente et al., 1998). A now rather dated estimate for the British Isles put the annual incidence of B. divergens on the island of Ireland at 15,000 cases per year (Gray and Murphy, 1985).

Zoonoses and Food Safety

Human infections with Babesia divergens, B. microti, B. bovis, or B. canis have been reported (Gorenflot et al., 1998). In Yugoslavia B. bovis was incriminated (Skrabalo and Deanovic, 1957), in Ireland B. divergens, and in northeastern USA B. microti of rodents was the causal agent (Healy et al., 1976). In Europe the territorial range of the disease coincides with that of bovine babesiosis caused by B. divergens, for which cattle are reservoir hosts and the vector is Ixodes ricinus. B. microti is transmitted by I. dammini, which also transmits Borrelia burgdorferi, the agent of Lyme disease. Simultaneous B. microti and B. burgdorferi infections can occur in man (Nyindo, 1992).

Human babesiosis cases in Europe are very uncommon but require rapid aggressive treatment. In the past most have occurred in splenectomised patients and were caused by B. divergens. Parasitaemias may range between 1 and 80% causing severe intravascular haemolysis with haemoglobinuria. The subsequent nonspecific clinical presentation can be easily confused with malaria; jaundice due to severe hemolysis is accompanied by persistent nonperiodic high fever (40 to 41°C), shaking chills, intense sweats, headaches, and myalgia as well as lumbar and abdominal pain.

Vomiting and diarrhea may be present. Total hemoglobin levels may fall to 70 to 80 g/liter, In the most severe cases, patients develop shock-like symptoms, with renal failure induced by intravascular hemolysis and pulmonary edema (Gorenflot et al., 1998). Unless treated rapidly, the infection is usually fatal.

In contrast, hundreds of cases of human infection with Babesia (chiefly B. microti, but also several other as yet unidentified strains or species) have been reported in the USA.Depending on the immune status of the host, clinical manifestations of human B. microti infections range widely. Although they may be asymptomatic in an otherwise healthy individual, infections may be severe and even fatal in immunocompromized patients (Gorenflot et al., 1998). It has been suggested that inapparent or latent infections may be quite common. For example, Orsono (1975) found that approximately 38% of individuals in a rural endemic area of animal babesiosis in Mexico showed serological evidence of infection.

Since transmission of human babesiosis is through tick bites, fear of pathogen survival in meat, meat inspection and food hygiene are not a concern.

Disease Treatment

In the past, treatment of babesiosis was mainly by use of azo-dyes of benzidine group, quinuronium derivatives, acridine derivatives, diamidine derivatives (Hall, 1977; Morel, 1989; Nyindo, 1992) and tetracyclines (Sackey et al., 1989; Pipano et al., 1988). The trypan blue and trypan red (azo-dyes) were the first drugs introduced for the treatment of babesiosis, but were withdrawn when more effective drugs were discovered (Nyindo, 1992). The quinuronium derivatives widely used in the past for the treatment of babesiosis include acaprin, babesan, piroplamin, pirevan and piroparv; whereas the acridine derivatives commonly used are acriflavine, gonacrine and flavin. The diamidine derivatives used include stilbamidine, propamidine, phenamidine, berenil and diamprone. A number of effective babesicides have been identified. However, because of residue and safety concerns their use is restricted in most countries. Diminazene aceturate is active against Babesia spp. in cattle, sheep, horses and dogs (Peregrine, 1994). It is marketed under trade names such as Berenil, Veriben or Ganaseg and is widely used in the tropics as both a babesicide and a trypanocide. Diminazene does not eliminate B. bovis or B. divergens, but it can eliminate B. bigemina. Quinuronium sulfate is very fast and effective but also the most toxic babesicide, affecting the parasympathetic nervous system. It was extensively used as a babesiacide until the 1940s when it was withdrawn because of its narrow therapeutic index (see Table). However, in the Middle East, it is still commonly used for ovine babesiosis. It is given at a single dose of 1 mg/kg bodyweight intramuscularly (BW i.m.) (Hall, 1977). It is also useful in treating pigs. The only drug licensed for use in the USA, Australia and most of Europe is imidocarb diproprionate. It is the drug of choice for infection with B. bigemina, B. bovis, B.divergens B. canis and B. gibsoni. Furthermore, unlike the other compounds that are marketed as babesiacides, imidocarb has significant prophylactic activity against Babesia spp., especially B. bigemina, which generally lasts 4-6 weeks (Peregrine, 1994). It is marketed as Imizol or Carbesia (Wellcome). Because of its persistence in tissues it has a withholding period in cattle and restrictions apply to its use in dairy cattle. Tetracyclines, both short-acting and long-acting preparations, have been useful as a prophylactic treatment against babesiosis at the dose rate of 5-20 mg/kg BW i.m. (Peregrine, 1994). Animals that are exposed to Babesia during the period of prophylaxis develop protective immunity (Urquhart et al., 1996).

In the past, the persistence of small numbers of parasites in the bloodstream was deemed necessary for the maintenance of resistance to reinfection. Today the concept of premunition is no longer accepted. While a certain period of antigenic exposure is necessary before treatment to facilitate the establishment of immunity, cattle treated with imidocarb diproprionate end up with a solid sterile immunity (Lewis et al., 1981). Long- term persistence of low-level parasitaemia is now considered a disadvantage. Remaining parasites may give rise to recrudescence under adverse conditions, treated cattle may act as a source of infection (Purnell et al., 1981), and parasites surviving at low levels of babesicide may acquire resistance.

Drug therapy of babesiosis

* average activity
** good activity
*** excellent activity

In spite of these concerns, drug resistance has yet to constitute a constraint to the efficacy of the compounds that are currently used for babesiosis (Peregrine, 1994). The withdrawal of drugs previously used for babesiosis has not been due to drug resistance, but because of a decline in demand and residue concerns. The choice of drug for treatment of babesiosis thus depends on the Babesia species involved and tick/disease status of the area. Information on medicinal plants and herbal preparations effective in the treatment of babesiosis is starting to emerge (Kasahara et al., 2005; Subeki et al., 2005).

Prevention and Control

The veterinary importance of babesiosis is chiefly that it acts as a constraint to the introduction of improved livestock from other areas (Urquhart et al.,1996). Control of babesiosis is based on several factors: elimination of the tick vector, complete elimination of the protozoan, control of the protozoan by maintaining a state of enzootic stability (Hall, 1977), vaccination (Barriga, 1994) and rearing of tick-resistant animals (Urquhart et al., 1996).

Recent advances in immunology and biotechnology have stimulated much research on the control of parasitic diseases through vaccination. Vaccination is carried out by administration of live vaccines, dead whole parasites, crude parasite extract or recombinant vaccines. Alternatively animals may be immunized by exposure to natural tick infestation while they are protected by colostrum, inverse age resistance and/or prophylaxis. Live vaccines derived from splectomized calves are widely used in Australia (Bock et al., 2004). Animals may be immunized by injecting them with infected blood and controlling the ensuing infection with babesiacidal drugs (Morel, 1989; Nyindo, 1992). Alternatively vaccine strains with reduced pathogenicity are used. Numerous Babesiaantigens that generate partial protection have been produced as recombinant proteins (Fukumoto et al., 2005; Schetters, 2005). A commercial vaccine against canine babesiosis with an efficiency of about 89% is available in France (Nyindo, 1992; Barriga, 1994).

Tick control, an important component of babesiosis control, may involve the used of acaricides (Urquhart et al., 1996) or the use of vaccines against the ticks.

In the areas requiring only Boophilus control (Australia, tropico-equatorial America, Asia), the minimum treatment frequency is fortnightly in the hot season and monthly in the cold season. Elsewhere (such as tropico-equatorial Africa, Mediterranean region) where tick species simultaneously parasitize cattle and transmit Babesia, treatment should be given weekly during the period of adult activity. In cattle, the selection and breeding of cattle that acquire a high degree of resistance to ticks can be practised (Urquhart et al., 1996).

Tick control in Western Europe in cattle herds is usually confined to hand spraying when, on infrequent occasions, large populations are observed, or when cattle are moved from endemic to tick-free areas. In contrast, in endemic areas in the British Isles, sheep are routinely dipped each spring (Urquhart et al., 1996).

Boophilus ticks with an occult tick gut recombinant antigen seem to have potential in inhibiting reproduction of the tick, but salivary antigens appear to be more effective at inhibiting feeding and pathogen transmission (Barriga, 1994).

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