- Host Animals
- Hosts/Species Affected
- Systems Affected
- Distribution Table
- List of Symptoms/Signs
- Disease Course
- Impact: Economic
- Zoonoses and Food Safety
- Disease Treatment
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
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
Pathogen/sTop of page
OverviewTop of page
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 cause
s 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).
Host AnimalsTop of page
|Animal name||Context||Life stage||System|
|Bos indicus (zebu)||Domesticated host||Cattle and Buffaloes|All Stages|
|Bos taurus (cattle)||Domesticated host||Cattle and Buffaloes|All Stages|
|Bubalus bubalis (Asian water buffalo)||Domesticated host||Cattle and Buffaloes|Bull; Cattle and Buffaloes|Cow; Cattle and Buffaloes|Heifer; Cattle and Buffaloes|Ox; Cattle and Buffaloes|Steer|
|Canis familiaris (dogs)||Domesticated host||Other|Adult Female; Other|Adult Male|
|Capra hircus (goats)||Domesticated host||Sheep and Goats|All Stages|
|Cervidae||Domesticated host; Wild host||Other|All Stages|
|Equus asinus (donkeys)||Domesticated host||Other|All Stages|
|Equus caballus (horses)||Domesticated host||Other|All Stages|
|Felis catus (cat)||Domesticated host; Wild host||Other|Adult Female; Other|Adult Male|
|mules||Domesticated host||Other|All Stages|
|Ovis aries (sheep)||Domesticated host||Sheep and Goats|All Stages|
|Sus scrofa (pigs)||Domesticated host; Wild host||Pigs|All Stages|
Hosts/Species AffectedTop of page
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).
Systems AffectedTop of page
blood and circulatory system diseases of pigs
blood and circulatory system diseases of small ruminants
digestive diseases of large ruminants
digestive diseases of pigs
digestive diseases of small ruminants
multisystemic diseases of large ruminants
multisystemic diseases of pigs
multisystemic diseases of small ruminants
urinary tract and renal diseases of large ruminants
urinary tract and renal diseases of pigs
urinary tract and renal diseases of small ruminants
DistributionTop of page
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
|Organism||Animals affected||Geographical distribution||Tick vectors|
|Babesia bigemina||CattleZebuWater buffaloDeerWild ruminants||Central and South AmericaAustraliaAfricaSouthern EuropeChina||Boophilus annulatusB. microplusB. australisB. calcaratusB. decoloratusRhipicephalusevertsRh. bursaRh. appendiculatusHaemaphysalis punctata|
|Babesia bovis||CattleReindeerStagWater buffalo, wild ruminants||Southern EuropeAsiaAfricaAmericaAustralia||Ixodes ricinusI. persulcatusB. calcaratusRh. bursa|
|Babesia argentina||Cattle||Central and South AmericaAustralia||B. microplus|
|Babesia divergens||Cattle||Northern Europe||I. ricinus|
|Babesia canis||DogWolfJackalOther wild canids||AsiaAfricaSouthern EuropeUnited StatesCentral and Southern Americaformer Soviet Union||Rh. sanguineusD. reticulatusD. marginatusHa. leachiHy. plumbeum|
|Babesia gibsoni||DogWolfFoxJackal||IndiaSri LankaChinaTurkestanNorth Africa||Ha. bispinosaRh. sanguineus|
|Babesia equi||HorseMuleDonkeyZebra||AsiaAfricaUnited StatesEuropeSouth Americaformer Soviet Union||D .reticulatus,D .marginatus,,Rh. bursa,Rh .sanguineus,Rh.evertsi,Hyalomma excavatum,Hy.plumbeumHy.dromedarii|
|Babesia caballi||HorsesDonkeyMule||Southern EuropeAsiaformer Soviet UnionAfricaPanamaUnited StatesAustralia||D. marginatusD. silvarumD. nitensHy. excavatumHy. dromedariiHy. scupenseRh. bursaRh. sanguineusD. reticulatus|
|Babesia motasi||SheepGoats||Southern EuropeMiddle Eastformer Soviet UnionAsiaAfrica||D. silvarumHa. punctataRh. bursa|
|Babesia ovis||SheepGoats||TropicsSouthern EuropeMiddle EastAfrica Asiaformer Soviet Union||Rh. bursa|
|Babesia trautmanni||PigWarthogBush Pig||Southern Europeformer Soviet UnionAfricaChina||Rh. turanicusRh. sanguineusB. decoloratusD. reticulatus|
|Babesia felis||Domestic CatWild CatLionLeopardPumaAmerican Lynx||SudanSouth AfricaUnited States||UnknownHa. laechi?|
|Babesia major||Cattle||West and South EuropeUKNW AfricaChina||H. punctata|
|Babesia microti||Rodents||EuropeAmerica||Ixodes spp|
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
Distribution TableTop of page
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.Last updated: 10 Jan 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Algeria||Absent, No presence record(s)|
|Angola||Absent, No presence record(s)|
|Cabo Verde||Absent, No presence record(s)|
|Cameroon||Absent, No presence record(s)|
|Central African Republic||Present|
|Congo, Republic of the||Absent, Unconfirmed presence record(s)|
|Eritrea||Absent, No presence record(s)|
|Mauritius||Absent, No presence record(s)|
|Seychelles||Absent, No presence record(s)|
|Tunisia||Absent, No presence record(s)|
|Armenia||Absent, No presence record(s)|
|Azerbaijan||Absent, No presence record(s)|
|Bhutan||Absent, No presence record(s)|
|Brunei||Present||CAB Abstracts Data Mining|
|-Tibet||Present||Original citation: Suolangcidan, and Qiong (1998)|
|-Jammu and Kashmir||Present|
|-Lesser Sunda Islands||Present||Native|
|Japan||Absent, No presence record(s)||1993|
|Kazakhstan||Absent, No presence record(s)|
|Kuwait||Absent, No presence record(s)|
|Kyrgyzstan||Absent, No presence record(s)|
|Laos||Absent, No presence record(s)|
|-Sarawak||Present||CAB Abstracts Data Mining|
|Nepal||Absent, No presence record(s)|
|North Korea||Absent, No presence record(s)|
|Saudi Arabia||Absent, No presence record(s)|
|Singapore||Absent, No presence record(s)|
|South Korea||Absent, No presence record(s)||2004|
|Tajikistan||Absent, No presence record(s)|
|Thailand||Absent, No presence record(s)|
|Uzbekistan||Absent, No presence record(s)|
|Vietnam||Absent, Unconfirmed presence record(s)|
|Belgium||Absent, No presence record(s)|
|Bosnia and Herzegovina||Absent, No presence record(s)|
|Bulgaria||Absent, No presence record(s)||2005|
|Croatia||Absent, No presence record(s)|
|Cyprus||Absent, No presence record(s)|
|Czechia||Absent, No presence record(s)|
|Denmark||Absent, No presence record(s)|
|Estonia||Absent, No presence record(s)|
|Germany||Absent, No presence record(s)||2007|
|Iceland||Absent, No presence record(s)|
|Italy||Absent, No presence record(s)||2004|
|Jersey||Absent, No presence record(s)|
|Latvia||Absent, No presence record(s)|
|Liechtenstein||Absent, No presence record(s)|
|Lithuania||Absent, No presence record(s)|
|Luxembourg||Absent, No presence record(s)|
|Malta||Absent, No presence record(s)|
|Moldova||Absent, No presence record(s)|
|Montenegro||Absent, No presence record(s)|
|North Macedonia||Absent, Unconfirmed presence record(s)|
|Norway||Absent, No presence record(s)||2008||Last reported: 200806|
|Portugal||Absent, No presence record(s)|
|Romania||Absent, No presence record(s)||2004|
|Serbia||Absent, No presence record(s)|
|Serbia and Montenegro||Absent, No presence record(s)|
|Slovakia||Absent, No presence record(s)|
|Spain||Absent, No presence record(s)|
|Switzerland||Absent, No presence record(s)|
|Ukraine||Absent, No presence record(s)|
|United Kingdom||Present, Localized|
|Bermuda||Absent, No presence record(s)|
|British Virgin Islands||Absent, No presence record(s)|
|Canada||Absent, No presence record(s)|
|Cayman Islands||Absent, No presence record(s)|
|Curaçao||Absent, No presence record(s)|
|Dominican Republic||Present, Localized|
|Greenland||Absent, No presence record(s)|
|Guadeloupe||Absent, Unconfirmed presence record(s)|
|Haiti||Absent, Unconfirmed presence record(s)|
|Honduras||Absent, No presence record(s)|
|Jamaica||Absent, No presence record(s)||2004|
|Saint Kitts and Nevis||Present||Native|
|Saint Vincent and the Grenadines||Present|
|United States||Absent, No presence record(s)|
|-Minnesota||Present||Original citation: Peirini et al. (1995)|
|New Caledonia||Present, Localized|
|New Zealand||Absent, No presence record(s)|
|Papua New Guinea||Present|
|Vanuatu||Absent, No presence record(s)|
|-Bahia||Present||Original citation: Aranjo et al. (1998)|
|-Mato Grosso do Sul||Present|
|-Rio de Janeiro||Present, Widespread|
|-Rio Grande do Sul||Present|
|Chile||Absent, No presence record(s)|
|Ecuador||Absent, No presence record(s)|
|Falkland Islands||Absent, No presence record(s)|
|French Guiana||Absent, No presence record(s)|
|Peru||Absent, Unconfirmed presence record(s)|
PathologyTop of page
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).
DiagnosisTop of page
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).
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).
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.
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/SignsTop of page
|Cardiovascular Signs / Tachycardia, rapid pulse, high heart rate||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Diagnosis|
|Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Digestive Signs / Ascites, fluid abdomen||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Digestive Signs / Decreased amount of stools, absent faeces, constipation||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Digestive Signs / Diarrhoea||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Digestive Signs / Grinding teeth, bruxism, odontoprisis||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Diagnosis|
|Digestive Signs / Hepatosplenomegaly, splenomegaly, hepatomegaly||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Diagnosis|
|Digestive Signs / Melena or occult blood in faeces, stools||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Digestive Signs / Rumen hypomotility or atony, decreased rate, motility, strength||Sign|
|General Signs / Ataxia, incoordination, staggering, falling||Cattle and Buffaloes|All Stages; Other|All Stages||Sign|
|General Signs / Decreased, absent thirst, hypodipsia, adipsia||Cattle and Buffaloes|All Stages||Diagnosis|
|General Signs / Dehydration||Sign|
|General Signs / Dysmetria, hypermetria, hypometria||Sign|
|General Signs / Exercise intolerance, tires easily||Cattle and Buffaloes|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|General Signs / Fever, pyrexia, hyperthermia||Cattle and Buffaloes|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Diagnosis|
|General Signs / Generalized weakness, paresis, paralysis||Sign|
|General Signs / Hypothermia, low temperature||Sign|
|General Signs / Icterus, jaundice||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Diagnosis|
|General Signs / Inability to stand, downer, prostration||Sign|
|General Signs / Lack of growth or weight gain, retarded, stunted growth||Cattle and Buffaloes|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|General Signs / Lymphadenopathy, swelling, mass or enlarged lymph nodes||Cattle and Buffaloes|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|General Signs / Opisthotonus||Sign|
|General Signs / Orbital, periorbital, periocular, conjunctival swelling, eyeball mass||Other|All Stages||Diagnosis|
|General Signs / Pale mucous membranes or skin, anemia||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Diagnosis|
|General Signs / Paraparesis, weakness, paralysis both hind limbs||Other|All Stages||Sign|
|General Signs / Polydipsia, excessive fluid consumption, excessive thirst||Other|All Stages||Diagnosis|
|General Signs / Reluctant to move, refusal to move||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|General Signs / Sudden death, found dead||Other|All Stages||Sign|
|General Signs / Tetraparesis, weakness, paralysis all four limbs||Other|All Stages||Sign|
|General Signs / Trembling, shivering, fasciculations, chilling||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|General Signs / Weight loss||Cattle and Buffaloes|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Musculoskeletal Signs / Head, face, neck spasms, myoclonus||Cattle and Buffaloes|All Stages; Other|All Stages||Sign|
|Nervous Signs / Abnormal behavior, aggression, changing habits||Cattle and Buffaloes|All Stages||Diagnosis|
|Nervous Signs / Circling||Other|All Stages||Sign|
|Nervous Signs / Coma, stupor||Cattle and Buffaloes|All Stages; Other|All Stages||Sign|
|Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Nervous Signs / Excitement, delirium, mania||Cattle and Buffaloes|All Stages; Other|All Stages||Diagnosis|
|Nervous Signs / Hindlimb hypoesthesia, anesthesia rear leg||Other|All Stages||Diagnosis|
|Nervous Signs / Hyperesthesia, irritable, hyperactive||Cattle and Buffaloes|All Stages||Diagnosis|
|Nervous Signs / Seizures or syncope, convulsions, fits, collapse||Cattle and Buffaloes|All Stages; Other|All Stages||Diagnosis|
|Nervous Signs / Tremor||Cattle and Buffaloes|All Stages; Other|All Stages||Sign|
|Ophthalmology Signs / Abnormal pupillary shape or defect in the iris||Other|All Stages||Sign|
|Ophthalmology Signs / Chemosis, conjunctival, scleral edema, swelling||Other|All Stages||Diagnosis|
|Ophthalmology Signs / Corneal edema, opacity||Other|All Stages||Sign|
|Ophthalmology Signs / Decreased or absent menace response but not blind||Cattle and Buffaloes|All Stages||Sign|
|Ophthalmology Signs / Lacrimation, tearing, serous ocular discharge, watery eyes||Other|All Stages||Diagnosis|
|Ophthalmology Signs / Mydriasis, dilated pupil||Sign|
|Ophthalmology Signs / Nystagmus||Sign|
|Reproductive Signs / Abortion or weak newborns, stillbirth||Cattle and Buffaloes|Cow||Sign|
|Reproductive Signs / Agalactia, decreased, absent milk production||Cattle and Buffaloes|Cow; Pigs|Sow; Sheep and Goats|Mature female||Sign|
|Reproductive Signs / Galactorrhea, inappropriate milk production||Cattle and Buffaloes|Cow; Pigs|Sow; Sheep and Goats|Mature female||Sign|
|Respiratory Signs / Dyspnea, difficult, open mouth breathing, grunt, gasping||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Skin / Integumentary Signs / Rough hair coat, dull, standing on end||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Sign|
|Urinary Signs / Haemoglobinuria or myoglobinuria||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Diagnosis|
|Urinary Signs / Oliguria or anuria, retention of urine||Sign|
|Urinary Signs / Red or brown urine, pink||Cattle and Buffaloes|All Stages; Other|All Stages; Pigs|All Stages; Sheep and Goats|All Stages||Diagnosis|
Disease CourseTop of page
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).
EpidemiologyTop of page
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: EconomicTop of page
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 SafetyTop of page
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 TreatmentTop of page
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
|Drugs||Concentration||Route||B. bigemina||B. bovis B. divergens||B. caballi||B. equi|
|Diminazene aceturate||7%||i.mi.v.||2-4 mg/kg *** for treatment;7-10 mg/kg for sterilization;||5-6 mg/kg** for treatment;||2-4 mg/kg *** for treatment;7-10 for sterilization||5-6 mg/kg** for treatment;5 mg/ kg for premunition|
|Imidocarb dipropionate||12%||i.ms.c.||0.5-1 mg/kg ***for treatment;2 mg/kg for prophylaxis andsterility||1-2 mg/kg **for treatment;2-4 mg/kg for prophylaxis 2-5 mg/kg for sterilization||2 mg/kg*** for prophylaxis 2-4 mg/kg/dx2 at 72 h||5 mg/kg **for treatment;4 mg/kg/dx2 at 72h for sterilization|
|Quinuronium sulphate||5%||s.c.||0.5-0.75 mg/kg*||1 mg/kg*||0.3 mg/kg 2 at 6-hourly interval||-|
* 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 ControlTop of page
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).
ReferencesTop of page
Adam KMG; Blewett DA; Collins TJ; Edgar JT, 1978. Outbreaks of babesiasis on two farms in Scotland. British Veterinary Journal, 134:428-433.
African Union-Interafrican Bureau for Animal Resources, 2011. Panafrican Animal Health Yearbook 2011. Pan African Animal Health Yearbook, 2011:xiii + 90 pp. http://www.au-ibar.org/index.php?option=com_flexicontent&view=items&cid=71&id=109&Itemid=56&lang=en
Aguirre DH; Bermúdez AC; Mangold AJ; Guglielmone AA, 1990. Natural infections with Babesia bovis and Babesia bigemina in Hereford, Criolla and Nelore cattle in Tucumán, Argentina. Revista de Medicina Veterinaria (Buenos Aires), 71(2):54-60; 18 ref.
Al Hadethi H; Al Saffar TM, 1988. Prevalence of parasitic infections of sheep in Northern Iraq. Journal of Veterinary Parsitology, 2(2):93-95.
Alani AJ; Herbert IV, 1988. The morphometrics of Babesia motasi (Wales) and its transmission by Haemaphysalis punctata (Canestrini and Fanzago 1877) to sheep. Veterinary Parasitology, 30(2):87-95; 23 ref.
Alhassan A; Pumidonming W; Okamura M; Hirata H; Battsetseg B; Fujisaki K; Yokoyama N; Igarashi I, 2005. Development of a single-round and multiplex PCR method for the simultaneous detection of Babesia caballi and Babesia equi in horse blood. Veterinary Parasitology, 129:43-49.
Alonso M; Camus E; Rodriguez-Diego J; Bertaudiere L; Tatareau JC; Liabeuf JM, 1992. Current position of bovine haemoparasitoses bovines en Martinique (Antilles francaises). Revue d'Elevage et de Medecine Veterinaire des pays Tropicaux, 45(1):9-14.
Alvarez V; Perez E; Herrero MV; Camus E; House JA ed; Uilenberg G, 1996. Epizootologic instability of bovine population against Babesia bovis (Piroplasmida: Babesiidea) in the region of Poas, Costa Rica. Vector-borne pathogens: International Trade and Tropical Animal Diseases Conference held on May 8-12, 1995 in San Jose, Costa Rica. Annal of the New York Academy of Sciences, 791:110- 116.
Arai S; Tsuji M; Kim-Samju; Nakada K; Kirisawa R; Ohta M; Ishihara C; Kim SJ, 1998. Antigenic and genetic diversities of Babesia ovata in persistently infected cattle. Journal of Veterinary Medical Science, 60(12):1321-1327.
Araújo FR; Madruga CR; Leal CRB; Schenk MAM; Kessler RH; Marques APC; Lemaire DC, 1998. Comparison between enzyme-linked immunosorbent assay, indirect fluorescent antibody and rapid conglutination tests in detecting antibodies against Babesia bovis. Veterinary Parasitology, 74(2/4):101-108; 22 ref.
Ashmawy KE; El-Wafa SAA; Fadly RS, 1998. Incidence of Babesia bigemina infection in native breed cattle, Behera Province, Egypt using different methods of diagnosis. Assiut Veterinary Medical Journal, 39(77):110-120; 28 ref.
Atkas M; Altay K; Dumanli N, 2005. Development of polymerase chain reaction method for diagnosis of Babesia ovis infection in sheep and goats. Veterinary Parasitology, 133:277-281.
Baader C, 1988. Occurrence and importance of Babesia infection of cattle and small ruminants in France. Vorkommen und Bedeutung der Babesiose bei Rindern und kleinen Wiederkäuern in Frankreich., 103 pp.; 240 ref.
Bai Q; Liu GY; Zhang L; Zhou JY, 1990. Studies on the isolation and preservation of a single species of bovine haematocytozoon: the finding and isolation of Babesia ovata in China. Chinese Journal of Veterinary Medicine, 16(12):2-4; 20 ref.
Bai Qi; Liu Guangyuang; Liu Dekao; Ren Jiaxing; Li Xing, 2002. Isolation and preliminary characterization of a large Babesia sp. from sheep and goats in the eastern part of Gansu Province, China. Parasitology Research, 88(Suppl. 1):S16-S21; 13 ref.
Barbosa MFR; Costa JO; Tafuri WL, 1994. Congenital transmission of Babesia bovis: first autochthonous case in Minas Gerais, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 46(5):519-526; 10 ref.
Barci LAG; Oliveira MR; Machado RZ; Oliveira DA; Araújo Filho RS, 1994. Epidemiology of cattle babesiosis in the Sao Paulo State: I. Studies in dairy cattle of type B from Pindamonhagaba county, Paraiba Valley. Revista Brasileira de Parasitologia Veterinária, 3(2):79-82; 11 ref.
Basalo AR; Parra O; Arraga de Alvarado CM; León E; Guillén A, 1995. Establishment of the indirect immunofluorescence serological technique as a diagnostic method for bovine babesiosis in the diagnostic laboratory of the veterinary clinic at the University of Zulia. Revista Cientifica, Facultad de Ciencias Veterinarias, Universidad del Zulia, 5(2):87-94; 30 ref.
Ben Musa N; Dawoud HA, 2004. The protective activity of serum and fractionated serum from rats against Babesia divergens. Journal of the Egyptian Society for Parasitology, 34:407-22.
Ben Said MS, 1993. Babesiasis of goats in northern Tunisia. Epidemiological and clinical observations. Etudes et Synthèses de l'IEMVT, No.42:664-682.
Biu AA, 1997. Prevalence of Ectoparasites of cattle and the biology of Hyalomma species in Maiduguri, Nigeria. MSc. Thesis.
Bock R; Jackson L; Vos A de; Jorgensen W, 2004. Babesiosis of cattle. Parasitology, 129 Suppl, S247-69.
Bock RE; Jackson LA; Vos AJde; Jorgensen WK, 2008. Babesiosis of cattle. In: Ticks: biology, disease and control [ed. by Bowman, A. S.\Nuttall, P. A.]. Cambridge, UK: Cambridge University Press, 281-307.
Boonchit S; Alhassan A; Chan B; Xuan X; Yokoyama N; Ooshiro M; Goff WL; Waghela SD; Wagner G; Igarashi I, 2006. Expression of C-terminal truncated and full-length Babesia bigemina rhoptry-associated protein 1 and their potential use in enzyme-linked immunosorbent assay. Veterinary Parasitology, 137(1-2):28-35.
Boozer AL; Macintire DK, 2003. Canine babesiosis. Veterinary Clinics of North America: Small Animal Practice, 33(4):885-904.
Bossche Pvan den; Mudenge D, 1999. The effect of short-interval deltamethrin applications to control tsetse on the seroprevalence of babesiosis in cattle. Tropical Animal Health and Production, 31(4):215-222; 14 ref.
Braccini GL; Chaplin EL; Stobbe NS; Araújo FAP; Santos NR, 1992. Protozoology and rickettsial findings of the laboratory of the Veterinary Faculty of the Federal University of Rio Grande Do Sul, Brazil, 1986-1990. Arquivos da Faculdade de Veterinária, UFRGS, 20:134-149; 11 ref.
Brown WC, 2001. Molecular approaches to elucidating innate and acquired immune responses to Babesia bovis, a protozoan parasite that causes persistent infection. Veterinary Parasitology, 101(3/4):233-248; many ref.
Brown WC; Norimine J; Knowles DP; Goff WL, 2006. Immune control of Babesia bovis infection. Veterinary Parasitology [First International Forum on Babesiosis, Nice, France, 4-6 November 2004.], 138(1/2):75-87.
Brun HH; Christensson DA; Eide DM; Gronstol H, 1998. Experimental infection with Babesia divergens in cattle persistently infected with bovine virus diarrhoae virus. Journal of Veterinary Medicine Series-B, 45(5):269-277.
Buening GM; Figueroa JV; Hansen JW, 1994. Development and application of DNA probe and PCR diagnostic methods in bovine babesiosis: Babesia bigemina. In: Uilenber G, Permin A, ed. Use of applicable biotechnological methods for diagnosing haemoparasites. Proceedings of the expert consultation, Merida, Mexico, 4-6 October 1994. Rome, Italy: FAO, 38-45.
Böse R; Jorgensen WK; Dalgliesh RJ; Friedhoff KT; Vos AJde, 1995. Current state and future trends in the diagnosis of babesiosis. Veterinary Parasitology [Special Issue: Tick-borne hemoparasitic diseases of livestock.], 57(1/3):61-74.
Cardozo H; Solari MA; Etchebarne J; Larrauri JH, 1994. Seroepidemiological study of Babesia bovis in support of the Uruguayan Boophilus microplus control program. Revista Brasileira de Parasitologia Veterinária, 3(1):5-8; 17 ref.
Carrique JJ; Morales GJ; Edelsten M, 2000. Endemic instability for babesiosis and anaplasmosis in cattle in the Bolivian Chaco. Veterinary Journal, 160(2):162-164; 12 ref.
Carrique Mas JJ; Widdowson MA; Cuellar AM; Ribera H; Walker AR, 2000. Risk of babesiosis and anaplasmosis in different ecological zones of Santa Cruz department, Bolivia. Veterinary Parasitology, 93(1):29-38.
Chandrawathani P; Tsuji N; Kawazu S; Ishikawa M; Fujisaki K, 1994. Seroepidemiological studies of bovine babesiosis caused by Babesia ovata, B. bigemina and B. bovis in Peninsular Malaysia. Journal of Veterinary Medical Science, 56(5):929-932; 11 ref.
Chansiri L; Preston PM; Yin Hong, 1997. Tick-borne diseases in Thailand. Tropical Animal Health and Production, 29(4):(supplement), 535.
Christensson DA, 1987. Clinical and serological response after experimental inoculation with Babesia divergens of newborn calves with and without maternal antibodies. Acta Veterinaria Scandinavica, 28(3-4):381-392; 56 ref.
Ckmak A; Dincer S; Karer Z, 1991. Studies on the serological diagnosis of Babesia ovis infection in sheep in the Samsun area. Veteriner Fakultesi Dergisi, üniversitesi Ankara, 38(1-2):242-251; 36 ref.
Clark IA; Allison AC; Cox FE, 1976. Protection of mice against Babesia and Plasmodium with BCG. Nature, 259:309.
Cooke BM; Mohandas N; Cowman AF; Coppel RL, 2005. Cellular adhesive phenomena in apicomplexan parasites of red blood cells. Veterinary Parasitology, 30:273-95.
Court RA; Jackson LA; Lee RP, 2001. Elevated anti-parasitic activity in peripheral blood monocytes and neutrophils of cattle infected with Babesia bovis. International Journal for Parasitology, 31(1):29-37; 36 ref.
da Costa CL; Kohayagawa A; Dell Porto A; Bomfim SRM, 1997. Determination of anti-Babesia spp. antibody levels in buffalo calves (Bubalus bubalis) from birth to one year of age. Revista Brasileira de Parasitologia Veterinaria, 6(2):117-121.
Dantrakool A; Somboon P; Hashimoto T; Saito-Ito A, 2004. Identification of a new type of Babesia species in wild rats (Bandicota indica) in Chiang Mai Province, Thailand. Journal of Clinical Microbiology, 42:850-854.
Davies SFM; Joyner LP; Kendall SB, 1958. Studies on Babesia divergens (M’Fadyean & Stockman, 1911). Annals of Tropical Medicine and Parasitology, 52:206-215.
de Lima FVA; Molner E; Molnar L; Silva CMS; Lima FVA, 1999. Seroloepidemiological study of bovine babesiosis (Babesia bovis) by indirect ELISA test in the state of Para, Brazil. Revista de Ciencias Agrarias, No. 32, 55-64.
De Waal DT; Lopez Rebollar LM; Potgieter FT, 1992. The transovarial transmission of Babesia trautmanni by Rhipicephalus simus to domestic pigs. Onderstepoort Journal of Veterinary Research, 59(3):219-221; 23 ref.
De Waal DT; Potgieter FT; Combrink MP; Mason TE, 1990. The isolation and transmission of an unidentified Babesia sp. to cattle by Hyalomma truncatum Koch 1844. Onderstepoort Journal of Veterinary Research, 57(4):229-232; 22 ref.
Dipeolu OO, 1975. Survey of Tick infestation in trade cattle, sheep and goats in Nigeria. Bull. Anim. Health Prod. Afri., 23:165-172.
Donnelly J; Peirce MA, 1975. Experiments on the transmission of Babesia divergens to cattle by the tick Ixodes ricinus. International Journal for Parasitology, 5:363-367.
Dreyer K; Fowrie LJ; Kok DJ, 1998. Epidemiology of tick-bovine diseases of cattle in Botshabelo and Thaba Ndu in the Free State Province. Onderstepoort Journal of Veterinary Research, 65(4):285-289.
du Plessis JL; de Waal DT; Stoltss WH, 1994. A survey of the incidence and importance of the tick-borne diseases heartwater, redwater and anaplasmosis in the hearwater-endemic region of South Africa. Onderstepoort Journal of Veterinary Research, 61(4):295-301.
Dzikowski R; Deitsch K, 2006. Antigenic variation by protozoan parasites: insights from Babesia bovis. Molecular Microbiology, 59:364-366.
Edelhofer R; Weissenbacher E; Bergmann A; Kutzer E, 1998. Field trials to assess the formalin-inactivated killed vaccine against Babesia divergens currently used in Austria. Wiener Tierärztliche Monatsschrift, 85(12):404-409; 19 ref.
Egbe-Nwiyi TN; Chaudhari SUR, 1996. Haematological studies on haemoparasites of different breeds of cattle in arid zone of north-eastern Nigeria: preliminary observations. Pakistan Veterinary Journal, 16(3):149-151; 10 ref.
El-Seify MA; Eissa NA, 1990. Some clinico-pathological studies on cattle naturally infected with blood parasites in Beni-Suef Governorate. Egyptian Journal of Comparative Pathology and Clinical Pathology, 3(1):37-43.
Estrada-Pena A; Osacar JJ; Pichon B; Gray JS, 2005. Hosts and pathogen detection for immature stages of Ixodes ricinus (Acari: Ixodidae) in North-Central Spain. Experimental and Applied Acarology, 37:257-268.
Fadraga M; Cordovés CO; Puentes T, 1991. Circulation of antibodies to haemoparasites in cattle (Bos taurus) of high genetic value in Cuba. Revista Cubana de Ciencias Veterinarias, 22(3):249-255; 7 ref.
Figueroa JV; Alvarez JA; Ramos JA; Rojas EE; Santiago C; Mosqueda JJ; Vega CA; Buening GM, 1998. Bovine babesiosis and anaplasmosis follow-up on cattle relocated in an endemic area for hemoparasitic diseases. Annals of the New York Academy of Sciences, 849:1-10; 23 ref.
Fitzpatrick JEP; Kennedy CC; McGeown MG; Oreopouldous DG; Robertson JH; Soyannwo MA, 1968. Human case of Piroplasmosis (babesiosis). Nature, 217:861-862.
Flach EJ; Shambwana IA; Dolan TT; Kassim A; Pedersen H; Glass M; Morzaria SP, 1989. East Coast fever immunization trials on Unguja Island, Zanzibar. Theileriosis in eastern, central and southern Africa. Proceedings of a workshop on East Coast fever immunization held in Lilongwe, Malawi 20-22 September 1988, 77-82; 1 ref.
Foldvari G; Hell E; Farkas R, 2005. Babesia canis canis in dogs from Hungary: detection by PCR and sequencing. Veterinary Parasitology, 127:221-6.
Francis J, 1966. Resistance of Zebu and other cattle to tick infestation and babesiosis with special reference to Australia, and historical review. British Vet. J., 122:301-307.
Freidhoff KT; Ganse-Dumrath D; Weber C; Dumrath DG, 1988. Epidemiology and prophylaxis of babesiosis (Babesia divergens) in cattle. Symposium "Weideparasitosen Bad Zwischenahn, 17 und 18 September 1987, Kurz fassung der Vortrage, 52-56.
Friedhoff KT, 1993. Epidemiology and control of babesiosis (Babesia divergens) of cattle in Germany. Parasitosen von Rind und Schaf: Tagung der Fachgruppe "Parasitologie und Parasitäre Krankheiten", Husum, Germany, am 6. und 7. April 1992., 23-27; 8 ref.
Friedhoff KT; Soulé C, 1996. An account on equine babesioses. Revue Scientifique et Technique - Office International des épizooties, 15(3):1191-1201; 43 ref.
Fuente J de la; Rodriguez M; Redondo M; Montero C; Garcia-Garcia JC; Mendez L; Serrano E; Valdes M; Enriquez A; Canales M; Ramos E; Boue O; Machado H; Lleonart R; Armas CA de; Rey S; Rodriguez JL; Artiles M; Garcia L, 1998. Field studies and cost-effectiveness analysis of vaccination with Gavac against the cattle tick Boophilus microplus. Vaccine, 16:366-73.
Fukumoto S; Tamaki Y; Shirafuji H; Harakawa S; Suzuki H; Xuan X, 2005. Immunization with recombinant surface antigen P50 of Babesia gibsoni expressed in insect cells induced parasite growth inhibition in dogs. Clinical Diagnostic Laboratory Immunology, 12:557-9.
Gaffar FR; Franssen FFJ; Vries E de, 2003. Babesia bovis merozoites invade human, ovine, equine, porcine and caprine erythrocytes by a sialic acid-dependent mechanism followed by developmental arrest after a single round of cell fission. International Journal for Parasitology, 33:1595-603.
Gaido AB; Aguirre DH; Echaide STde; Guglielmone AA, 1997. Clinical incidence of primary Babesia bovis infections in dairy cattle in the Lerma Valley, Province of Salta, Argentina. Veterinaria Argentina, 14(137):460-463; 9 ref.
Garcia-Cuadrado N; Lopez de Torre G, 1993. Sanitary aspects of beef cattle farming: Parasitoses Junta de Extremadura, Merida, Spain, 303-330.
Ghimire NP, 1989. Concurrent babesiosis and trypanosomiasis of cattle in Nepal. Bangladesh Veterinarian, 6(1):50-51; 5 ref.
Gitau GK; Perry BD; Katende JM; McDermott JJ; Morzaria SP; Young AS, 1997. The prevalence of serum antibodies to tick-borne infections in cattle in smallholder dairy farms in Murang'a District, Kenya; a cross-sectional study. Preventive Veterinary Medicine, 30(2):95-107; 24 ref.
Goff WL; Johnson WC; Horn RH; Barrington GM; Knowles DP, 2003. The innate immune response in calves to Boophilus microplus tick transmitted Babesia bovis involves type 1 cytokine induction and NK-like cells in the spleen. Parasite Immunology, 25:185-188.
Goff WL; Johnson WC; Parish SM; Barrington GM; Elsasser TH; Davis WC; Valdez RA, 2002. IL-4 and IL-10 inhibition of IFN-
Goff WL; Johnson WC; Tuo W; Valdez RA; Parish SM; Barrington GM; Davis WC, 2002. Age-related innate immune response in calves to Babesia bovis involves IL-12 induction and IL-10 modulation. Annals of the New York Academy of Science, 969:164-8.
Gonçalves Ruiz PM; Passos LMF; Machado RZ; Lima JD; Ribeiro MFB, 2001. Development of an enzyme-linked immunosorbent assay for detection of IgM antibodies to Babesia bigemina in cattle. Memórias do Instituto Oswaldo Cruz, 96(2):237-240; 18 ref.
Gorenflot A; Brasseur P; Precigout E; L'Hostis M; Marchand A; Schrevel J, 1991. Cytological and immunological responses to Babesia divergens in different hosts: ox, gerbil, man. Parasitology Research, 77(1):3-12; 30 ref.
Gray JS, 1980. Studies on the activity of Ixodes ricinus in relation to the epidemiology of babesiosis in Co Meath, Ireland. British Veterinary Journal, 136:427-436.
Gray JS, 2006. Identity of the causal agents of human babesiosis in Europe. International Journal of Medical Microbiology [Proceedings of VIII International Potsdam Symposium on Tick-borne Diseases, Jena, Germany, 10-12 March, 2005.], 296S1(Supplement 40):131-136. http://www.sciencedirect.com/science/journal/14384221
Gray JS; Murphy TM; Taylor SM; Blewett DA; Harrington R, 1990. Comparative morphological and cross transmission studies with bovine and deer babesias in Ireland. Preventive Veterinary Medicine, 9(3):185-193; 13 ref.
Gueye A; Mbengue M; Diouf A, 1989. Ticks and haemoparasitoses of livestock in Senegal. IV. The south-Sudanian zone. Revue d'élevage et de Médecine Vétérinaire des Pays Tropicaux, 42(4):517-528; 14 ref.
Guglielmone AA; Aguirre DH; Späth EJA; Gaido AB; Mangold AJ; Ríos LGde, 1992. Long-term study of incidence and financial loss due to cattle babesiosis in an Argentinian dairy farm. Preventive Veterinary Medicine, 12(3-4):307-312; 12 ref.
Guglielmone AA; Echaide STde; Pérez y Santaella M; Iglesias JA; Vanzini VR; Lugaresi CI; Dellepiane EL, 1997. Cross-sectional estimation of Babesia bovis antibody prevalence in an area of Argentina used for extensive cattle breeding as an aid to control babesiosis. Preventive Veterinary Medicine, 30(2):151-154; 16 ref.
Guglielmone AA; Lugaresi CI; Volpogni MM; Anziani OS; Vanzini VR, 1997. Babesial antibody dynamics after cattle immunisation with live vaccines, measured with an indirect immunofluorescence test. Veterinary Parasitology, 70(1/3):33-39; 27 ref.
Ha TH; Nguyen DK; Phan DL; Pham SL, 1996. Observation on hemosporidian infection in dairy cattle in the Hanoi area. Khoa-Hoc-Ky-Thuat-Thu-Y, 3:61-64.
Hall HTB, 1977. Diseases and Parasites of Livestock in the Tropics. Payne WJA, ed. Hong Kong: Longman Group Ltd, 145-151.
Hardeng F, 1991. Epidemiology of diseases transmitted by ticks. A review with special emphasis on diseases transmitted by Ixodes ricinus in ruminants in Norway. Norsk Veterinærtidsskrift, 103(10):913-921; 18 ref.
Harper GS; Riddles PW; Waltisbuhl DJ; Wright IG, 1994. Applications of recombinant DNA technologies in the development of a vaccine: examples in the development of a vaccine against Babesia. Vaccines in agriculture: immunological applications to animal health and production., 161-169; 57 ref.
Healy GR; Spielman A; Gleason N, 1976. Human babesiosis: reservoir of infection on Nantucket Island, Science, 192:479-480.
Hong Y; Wenshun L; Jianxun L, 1997. Babesiosis in China. Tropical Animal Health and Production, 29: 11S-15S.
Huang DS; Huang DS; Preston PM, ed. , Yin Hong, 1997. An investigation into the piroplasma of domestic animals in Yunnan Province, China. Proceedings of the European Union International Symposium on ticks and tick-borne diseases, September 2-6, 1996. Xian, China.
Hugh JME; Scotland K; Applewhaite LM; Alexander FM, 1988. Seroprevalence of anaplasmosis and babesiosis in livestock on St. Lucia, 1983. Tropical Animal Health and Production, 20:137-139.
Hunfeld KP; Hildebrandt A; Gray JS, 2008. Babesiosis: recent insights into an ancient disease. International Journal for Parasitology, 38(11):1219-1237. http://www.sciencedirect.com/science/journal/00207519
Igarashi I; Aikawa M; Kreier JP, 1988. Host cell-parasite interactions in babesiosis In: Ristic M, ed. Babesiosis of Domestic Animals and Man. Boca Raton, Fla, USA: CRC Press, 53-69; 61 ref.
Jenkins MC, 2001. Advances and prospects for subunit vaccines against protozoa of veterinary importance. Veterinary Parasitology, 101:291-310.
Jithendran KP, 1977. Blood Protista of cattle and buffaloes in Kangra valley, Himachal Pradesh. Indian Journal of Animal Sciences, 63(3):207-208.
Jorgensen W; Weilgama DJ; Navaratne M; Weerasinghe C; Perera PSG, 1988. Observations on the prevalence of Babesia and Anaplasma infections in some Government livestock farms in Sri Lanka. Sri Lanka Veterinary Journal, 36:56-57.
Jorgensen WK; Weilgama DJ; Navaratne M; Dalgliesh RJ, 1992. Prevalence of Babesia bovis and Anaplasma marginale at selected localities in Sri Lanka. Tropical Animal Health and Production, 24(1):9-14; 7 ref.
Kakoma I; Mehlhorn H, 1994. Babesia of Domestic Animals, In: Krier JP, ed. Parasitic Protozoa. Volume 7. Academic Press Inc, 141-216.
Kang YB; Jang H, 1988. Parasitaemia induced by splenectomy in a calf naturally infected with Theileria sergenti and Babesia ovata.. Research Reports of the Rural Development Administration, Veterinary, Korea Republic, 30(2):7-11; 26 ref.
Kasahara K; Nomura S; Subeki; Matsuura H; Yamasaki M; Yamato O; Maede Y; Katakura K; Suzuki M; Trimurningsih; Chairul; Yoshihara T, 2005. Anti-babesial compounds from Curcuma zedoaria. Planta Medica, 71:482-484.
Katsande TC; More SJ; Bock RE; Mabikacheche L; Molloy JB; Ncobe C, 1999. A Serological survey of bovine babesiosis in Northern and Eastern Zimbabwe. Ondersterpoort Journal of Veterinary Research, 66(4):255-263.
Kjemtrup AM; Thomford JW; Gardner IA; Conrad PA; Jessup DA; Boyce WM, 1995. Seroprevalence of two Babesia spp. isolates in selected bighorn sheep (Ovis canadensis) and mule deer (Odocoileus hemionus) populations in California. Journal of Wildlife Diseases, 31(4):467-471; 17 ref.
Koch HT; Kambeva L; Ocama JGR; Munatswa FC; Franssen FFJ; Uilenberg G; Dolan TT; Norval RAI, 1990. Immunization of cattle against Theileria parva bovis and their exposure to natural challenge. Veterinary Parasitology, 37(3-4):185-196; 26 ref.
Komoin-Oka C; Zinsstag J; Pandey VS; Fofana F; N'Depo A, 1999. Epidemiology of parasites of sheep in the southern forest zone of Côte d'Ivoire. Revue d'élevage et de Médecine Vétérinaire des Pays Tropicaux, 52(1):39-46; 31 ref.
Lawrence JA; Musisi FL; Mfitilodze MW; Tjornehoj K; Whiteland AP; Kafuwa PT; Chamambala KE, 1996. Integrated tick and tick-borne disease control trials in crossbred dairy cattle in Malawi. Tropical Animal Health and Production, 28(4):280-288; 10 ref.
LeRoith T; BraytonKA; Molloy JB; BockRE; Hines SA; Lew AE; McElwain TF, 2005. Sequence variation and immunologic cross-reactivity among Babesia bovis merozoite surface antigen 1 proteins from vaccine strains and vaccine breakthrough isolates. Infection and Immunity, 73:5388-5394.
Levine ND, 1961. Protozoan Parasites of Domestic Animals and Man. Minneapolis, Mirr; Burgess Publishing Company. Pp.111-412.
Lew AE; Bock RE; Croft JM; Minchin CM; Kingston TG; Dalgliesh RJ, 1997. Genotypic diversity in field isolates of Babesia bovis from cattle with babesiosis after vaccination. Australian Veterinary Journal, 75(8):575-578; 9 ref.
Lewis D; Young ER, 1980. The transmission of a human strain of Babesia divergens by Ixodes ricinus ticks. Journal of Parasitology, 66:359-360.
Lewis DRE; Purnell LMA; Young ER, 1981. The effect of treatment with imidocarb dipropionate on the course of Babesia divergens infections in splenectomised calves, and their subsequent immunity to homologous challenge. Journal of Comparative Pathology, 91:285-292.
L-Hostis M, 1998. Te colloque swile controle Epidemiologique des Maladies infectieuses Institut Pasteur de Paris, France. Medicine - et Maladies-Infectieuses, 28(5):Special:359-362.
Lian-Can; He Hucheng; Bai Qi; Han Genfeng; Liu Guang Yuan; Lian C; He HC; Bai Q; Han GF; Liu GY, 1997. A new large Babesia sp found in clinically affected sheep in China. Chinese Journal of Veterinary Science, 17(2):116-119.
Linhares GFC; Massard CL; Araujo JLde B; Alves LC, 1992. Serological survey of Babesia bigemina (Smith & Kilborne, 1893) and Babesia bovis (Babés, 1888) in cattle from the central western region of Brazil. Arquivos da Universidade Federal Rural do Rio de Janeiro, 15(1):85-91; 33 ref.
Loa CC; Adelson ME; Mordechai E; Raphaelli I; Tilton RC, 2004. Serological diagnosis of human babesiosis by IgG enzyme-linked immunosorbent assay. Current Microbiology, 49:385-389.
Lochouarn L; Fontenille D, 1999. ELISA detection of malaria sporozoites: false-positive results in Anopheles gambiae s.l. associated with bovine bloodmeals. Transactions of the Royal Society of Tropical Medicine and Hygiene, 93(1):101-102; 9 ref.
Lohr KF, 1973. Susceptibility of non splenectomized and splenectomized Sahiwal cattle to experimental Babesia bigemina infection. Zbl. Vet. Med., B20:52-56.
Lu WenXiang; Lu WanShun; Zhang QiCai; Luo JianXun; Yin Hong; Dou HuiFang, 1995. Survey of the species of tick-transmitted haemocytozoa of cattle and the distribution features in China. Chinese Journal of Veterinary Science and Technology, 25(8):13-16; 6 ref.
Lu WS; Yin H; Lu WX; Yu F; Zhang QC; Dou HF, 1988. Discovery of Babesia major in cattle and confirmation of its transmitting vector tick in China. Chinese Journal of Veterinary Science and Technology, No. 12:11-14; 13 ref.
Lu WS; Yin H; Lu WX; Zhang QC; Yu F; Dou HF, 1990. Experimental studies on transovarian transmission of Babesia major from bovines by the tick Haemaphysalis longicornis.. Chinese Journal of Veterinary Science and Technology, No. 6:5-6; 9 ref.
Ma LH; Liu ZL; Zao JL, 1989. An investigation of babesiosis in buffaloes in Hubei Province. 5. The experimental demonstration of the transovarian transmission of Babesia bovis by Rhipicephalus haemaphysaloides haemaphysaloides.. Acta Veterinaria et Zootechnica Sinica, 20(1):67-70; 6 ref.
Madruga CR; Braga MM; Oliveira DB; Massard CL; Soares CO; Oliveira DB, 2000. Prevalence of antibodoes against Babesia bovis (Babes 1888) and B. bigemina (Smith and Kilborne, 1893) (Apicomlexa:Babesiidae) in cattle from four municipalities of Rio de Janeiro State. Revista Brasileira de Ciencias Veterinaria, 7(2):113-116.
Madruga CR; Suarez CE; McElwain TF; Palmer GH, 1996. Conservation of merozoite membrane and apical complex B cell epitopes among Babesia bigemina and Babesia bovis strains isolated in Brazil. Veterinary Parasitology, 61(1/2):21-30; 29 ref.
Martin T; Epstoin V, 1999. The animal health status of the Solomon Islands, 1991, 34pp.
Mattioli RC; Bah M; Kora S; Cassama M; Clifford DJ, 1995. Susceptibility to different tick genera in Gambian N'Dama and Gobra zebu cattle exposed to naturally occurring tick infestations. Tropical Animal Health and Production, 27(2):95-105; 30 ref.
Mattioli RC; Janneh L; Corr N; Faye JA; Pandey VS; Verhulst A, 1997. Seasonal prevalence of ticks and tick-transmitted haemoparasites in traditionally managed N'Dama cattle with reference to strategic tick control in the Gambia. Medical and Veterinary Entomology, 11(4):342-348; 38 ref.
Mehlhorn H; Schein E; Voigt WP, 1980. Light and electronmicroscopic study on the developmental stages of Babesia canis within the gut of the tick Dermacentor reticulatus. J. Parasitology, 66:220.
Melendez RD; Forlano M; Camus E, ed. , House JA, ed., Uilenberg G, 1996. Incidence and intensity of Babesia spp sporokinetes in engorged Boophilus microplus from dairy herd in Venezuela, Vector-borne pathogens: International trade and tropical animal diseases, held on May 8-12, 1995 in San Jose, Costa Rica. Annals of the New York Academy of Sciences, 791:148-156.
Molloy JB; Bowles PM; Bock RE; Turton JA; Katsande TC; Katende JM; Mabikacheche LG; Waldron SJ; Blight GW; Dalgliesh RJ, 1998. Evaluation of an ELISA for detection of antibodies to Babesia bovis in cattle in Australia and Zimbabwe. Preventive Veterinary Medicine, 33(1/4):59-67; 11 ref.
Moltman UG; Mehlhorn H; Friedhoff KT, 1982. Ultrastructural study of the development of Babesia ovis (Piroplasmia) in the ovary of the vector tick Rhipicephalus bursa. J. Protozool, 29:30.
Morel P, 1989. Tick-borne diseases of livestock in Africa. In: Mira Shah-Fischer, Ralph R. Manual of Tropical Veterinary Parasitology, 299-460.
Mota RA; Soares PC; Silva F; Soares CO; Lopes CWG; Massard CL, 2000. Babesiosis in goats on Pernambuet State, Brazil. Revista Brasilara de Medicine Veterinaria, 22(2):78-80.
Mulei CM; Rege JEO, 1989. An examination of the incidences of East Coast Fever (ECF), anaplasmosis, and babesiosis in the bovine in Kabete area of Kiambu District of Kenya. Bulletin of Animal Health and Production in Africa, 37(3):213-216; 10 ref.
Munatswa FC; Dolan TT, 1989. Theileriosis in Zimbabwe. Proceedings of a workshop on East coast fever immunization held in Lilongwe, Malawi, 20-22 September, 1988. ILRAD.
Musisi FL; Quiroga JC; Ngulube B; Kanhai GK, 1989. An East Coast fever immunization field trial at Kasoba, Malawi. Theileriosis in eastern, central and southern Africa. Proceedings of a workshop on East Coast fever immunization held in Lilongwe, Malawi 20-22 September 1988, 71-76; 2 ref.
Nagore D; García-Sanmartín J; García-Pérez AL; Juste RA; Hurtado A, 2004. Identification, genetic diversity and prevalence of Theileria and Babesia species in a sheep population from Northern Spain. International Journal for Parasitology, 34:1059-1067.
Ndi C; Bayemi PH; Ekue FN; Tarounga B, 1991. Preliminary observations on ticks and tick-borne diseases in the North West Province of Cameroon. I. Babesiosis and anaplasmosis. Revue d'élevage et de Médecine Vétérinaire des Pays Tropicaux, 44(3):263-265; 17 ref.
Nevils MA; Figueroa JV; Turk JR; Canto GJ; Le V; Ellersieck MR; Carson CA, 2000. Cloned lines of Babesia bovis differ in their ability to induce cerebral babesiosis in cattle. Parasitology Research, 86(6):437-443; 14 ref.
Nguyen VH; Nhu VT; Ha TH; La MS, 1999. A preliminary study on application of Polymerase chain reaction in diagnosis of haemosporidiosis in cattle, Khoa Hoc Ky Thuat Thu Y Veterinary Sciences and Techniques, 6,(1):48.
Niepold J, 1990. Examination of cattle sera for simultaneous infection with Borrelia burgdorferi and Babesia divergens.. Untersuchung von Rinderseren auf das simultane Vorkommen von Infektionen mit Borrelien (Borrelia burgdorferi) und Babesien (Babesia divergens)., 89 pp.; 19 pp. of ref.
Nowak F, 1990. Epidemiological investigation of cattle herds in central Sinutal, Cordoba province, Colombia. Epidemiologische Untersuchungen in Rinderbeständen im mittleren Sinutal (Cordoba, Kolumbien)., 102 pp.; 13 pp. of ref.
Nyindo M, 1992. Animal diseases due to protozoa and rickettsia. Nairobi, Kenya: English Press, 67-77.
Ohta M; Kawazu S; Tsuji N; Terada Y; Kamio T; Fujisaki K, 1995. Rapid and sensitive method for detection of newly isolated Babesia parasite (Babesia sp. 1) in the anticipated vector-tick using the polymerase chain reaction technique. Journal of Protozoology Research, 5(3):108-117; 22 ref.
OIE Handistatus, 2002. World Animal Health Publication and Handistatus II (dataset for 2001). Paris, France: Office International des Epizooties.
OIE Handistatus, 2003. World Animal Health Publication and Handistatus II (dataset for 2002). Paris, France: Office International des Epizooties.
OIE Handistatus, 2004. World Animal Health Publication and Handistatus II (data set for 2003). Paris, France: Office International des Epizooties.
OIE Handistatus, 2005. World Animal Health Publication and Handistatus II (data set for 2004). Paris, France: Office International des Epizooties.
OIE, 2009. World Animal Health Information Database - Version: 1.4. World Animal Health Information Database. Paris, France: World Organisation for Animal Health. http://www.oie.int
OIE, 2012. World Animal Health Information Database. Version 2. World Animal Health Information Database. Paris, France: World Organisation for Animal Health. http://www.oie.int/wahis_2/public/wahid.php/Wahidhome/Home
Okamura M; Yokoyama N; Wickramathilaka NPALK; Takabatake N; Ikehara Y; Igarashi I, 2005. Babesia caballi and Babesia equi: implications of host sialic acids in erythrocyte infection. Experimental Parasitology, 110:406-11.
Orsono MB, 1975. Public health importance of babesiosis (Quoted by Ristic and Lewis, 1977).
Osman AM; Maroli M, ed. , Ghirotti M, ed., de Castro JJ, 1997. Major tick borne diseases of sheep and goats in the Sudan. Proceedings of FAO Expert consultation on ticks and tick-borne diseases of sheep and goats, Rome, Italy 29-30 September 1994. Parasitologia-Rome, 39:143-144.
Papadopoulos B, 1990. Ticks and piroplasms of domestic animals in the Macedonia region of Greece. Revue Suisse de Zoologie, 97(4):782; [In Zoologia '90, "Parasites in Biological Systems", Basel, 6-7 April 1990 (Annual Conference of the Swiss Zoological Society)].
Petrini KR; Holman PJ; Rhyan JC; Jenkins SJ; Wagner GG, 1995. Fatal babesiosis in an American woodland caribou (Rangifer tarandus caribou). Journal of Zoo and Wildlife Medicine, 26(2):298-305; 25 ref.
Pichon B; Egan D; Rogers M; Gray J, 2003. Detection and identification of pathogens and host DNA in un-fed host-seeking Ixodes ricinus L. (Acari: Ixodidae). Journal of Medical Entomology, 40:723-731.
Pino R; Salabarría FF, 1989. Prevalence of Babesia bigemina (Smith & Kilborne 1983) during the period January-May 1987 in the Provinces of Ciudad de la Habana and La Habana. Revista Cubana de Ciencias Veterinarias, 20(4):227-232; 20 ref.
Popa E, 1998. Ixodid tick vectors of babesiosis in animals in Romania Revista Romana de Medicina Veterinara, 8(2):61-67.
Prosperi S; Baldelli R; Fioravanti ML; Roda R; Galuppi R; Michelini S, 1990. Pasture and bovine health risks. II. Serological survey for brucellosis, Q fever, chlamydiosis and babesiosis. Obiettivi e Documenti Veterinari, 11:59-61; 19 ref.
Purnell R E; Lewis D; Young ER, 1981. Quinuronium sulphate for the treatment of Babesia divergens infections of splenectomised calves. Veterinary Record, 108:538-539.
Purnell RE; Gunter TD; Schröder J, 1989. Development of a prophylactic regime using long-acting tetracycline for the control of redwater and heartwater in susceptible cattle moved into an endemic area. Tropical Animal Health and Production, 21(1):11-19; 19 ref.
Rabo JS; Jaryum J; Mohammed A, 1995. Outbreak of bovine babesiosis in Monguno Local Government Area of Borno state Nigeria:A case study, Annals of Borno 11/12:345-348.
Ribera Cuéllar H; Cuéllar AM; Barba Chávez G; Carrique-Mas JJ; Walker A, 2000. Study of babesiosis and anaplasmosis in relation to tick burdens of dairy calves in the eastern Bolivian lowlands. Veterinaria México, 31(1):39-46; 17 ref.
Riek RF, 1966. The life cycle of Babesia argentina (Lignieres, 1903) (Sporozoa: Piroplasmida) in the tick vector Boophilus microplus (Canestrini). Austr. J. Agric. Res., 17:247.
Ristic M; Lewis GE Jr, 1977. Babesia in man and wild and laboratory adapted mammals. In: Kreier JP, ed. Parasitic protozoa. New York, USA: New York Academic Press, 53-73.
Ristic M; Smith RD, 1974. Zoonoses caused by Haemoprotozoa. In parasitic zoonoses, ed. E. J.L. Soulsby New York Academic Press pp41-63.
Rosignoli C; Nigrelli AD; Savini G; Semproni G; Benaglia F; Franzini G, 2000. An outbreak of babesiosis (Babesia bovis) in a beef cattle fattening unit. Obiettivi e Documenti Veterinari, 21(3):65-70; 23 ref.
Sackey; AK; Agbede RIS; Abdullahi US, 1989. Effects of tetracycline on treatment of clinical babesiosis in intact cattle. Nigeria Livestock Farmer (NVRI, NAPRI, NAERALS, ABU Zaria), 9:1-4.
Sahibi H; Rhalem A; Berrag B; Goff WL; Jongejan F, ed. , Goff W, ed., Camus E, 1998. Bovine babesiosis. Seroprevalence and ticks associated with cattle from two different regions of Moroco. Annals of the New York Academy of Science, 849:213-218.
Salem GH, 1998. Using of ribosomal-DNA based PCR method for sensitive detection of carrier and mild babesial infections among cattle in Egypt. Assiut Veterinary Medical Journal, 39(78):92-108; 24 ref.
Salem GH, 1999. Diagnosis of both Babesia bovis and Babesia bigemina infections among carrier cattle by using extra-chromosal DNA based polymerase chain reaction test in Egypt. Assiut Veterinary Medical Journal, 42(83):38-54.
Schein E; Mehlhorn H; Voigt WP, 1979. Electron microspical studies on the development of Babesia canis (Sporozoa) in the salivary glands of the vector tick Dermacentor reticulatus. Acta Tropica, 36:229.
Schetters T, 2005. Vaccination against canine babesiosis. Trends in Parasitology, 21:179-184.
Serra Freire NM; Nuernberg S; da Serra-Freire NM, 1995. The cattle tick and babesiosis anaplasmosis in Santa Catarina State Brazil, Revista Brasileira de Medicine Veterinary, 17(6):257-259.
Shaw AA, 1989. Investigation on some infections in the exotic, pure and cross bred cattle of Kashmir valley. Indian Journal of Comparative Microbiology, Immunology and Infectious Diseases, 10(1):33-38; 17 ref.
Shiv-Prasad; Tripathi SC; Prasad S, 1999. Milk production in various categories of farmers families vis-à-vis seasonal variability of disease in Western plain of UP. Journal of Dairying Foods and Home Sciences, 18(2):124-126.
Shoda LK; Palmer GH; Florin-Christensen J; Florin-Christensen M; Godson DL; Brown WC, 2000. Babesia bovis-stimulated macrophages express interleukin-1beta, interleukin-12, tumor necrosis factor alpha, and nitric oxide and inhibit parasite replication in vitro. Infection and Immunity, 68:5139-5145.
Simoes Campos DA; Chirinos Rodríguez AR; Martínez de Chirinos NS; Castejón O; Avila JP, 1995. Prevalence of bovine babesiosis in Sector Cuatro (Playa Bonita), Mara county. Revista Cientifica, Facultad de Ciencias Veterinarias, Universidad del Zulia, 5(1):5-10; 30 ref.
Singh BB; Mbemba ZZ; Welu M; Butera M; Tolenga K, 1988. Epidemiological study of bovine piroplasmosis in north-eastern Zaire, particularly the north Kivu and Ituri subregions. Premières Journées Vétérinaires Africaines, Hammamet, Tunisie, 31 mai - 2 juin 1987., 127-139; 13 ref.
Skrabalo Z; Deanovic Z, 1957. Piroplasmosis in man. Report on a case. Doc. Med. Geogr. Trop., 9:11-16.
Smeenk I; Kelly PJ; Wray K; Musuka G; Trees AJ; Jongejan F, 2000. Babesia bovis and B. bigemina DNA detected in cattle and ticks from Zimbabwe by polymerase chain reaction. Journal of the South African Veterinary Association, 71(1):21-24.
Smith HA; Jones TC; Hunt RD, 1972. Veterinary Pathology, edition 4. Philadelphia, USA: Lea and Febiger, 723-726.
Smith RD; Evans DE; Martins JR; Ceresér VH; Correa BL; Petraccia C; Cardozo H; Solari MA; Nari A, 2000. Babesiosis (Babesia bovis) stability in unstable environments. Annals of the New York Academy of Sciences, 916:510-520; 16 ref.
Soares CO; Souza JCP; Madruga CR; Madureira RC; Massard CL; Fonseca AH, 2000. Seroprevalence of Babesia bovis in cattle in the Norte Fluminense region. Pesquisa Veterinária Brasileira, 20(2):75-79; 20 ref.
Solís-Calderón JJ; Rodríguez-Vivas RI; Dajer-Abimerhi A, 1998. Serological monitoring of IgG and IgM antibodies against Babesia bigemina (Haemosporidia: Babesiidae) in calves in the Mexican tropics. Revista de Biología Tropical, 46(4):1125-1130; 28 ref.
Solomon G; Kaaya GP; Gebreab F; Gemetchu T; Tilahun G, 1998. Ticks and tick-borne parasites associated with indigenous cattle in Didtuyura Ranch, southern Ethiopia. Insect Science and its Application, 18(1):59-66; 31 ref.
Solorio-Rivera JL; Rodríguez-Vivas RI; Pérez-Gutierrez E; Wagner G, 1999. Management factors associated with Babesia bovis seroprevalence in cattle from eastern Yucatán, Mexico. Preventive Veterinary Medicine, 40(3/4):261-269; 29 ref.
Soulsby EJL, 1986. Helminthss,Arthropods and Protozoa of Domesticated Animals, edition 7. London, UK: Bailliere Tindall, 706-728.
Subeki; Nomura S; Matsuura H; Yamasaki M; Yamato O; Maede Y; Katakura K; Suzuki M; Trimurningsih; Chairul; Yoshihara T, 2005. Anti-babesial activity of some central kalimantan plant extracts and active oligostilbenoids from Shorea balangeran. Planta Medica, 71:420-423.
Tarmudji; Siswansyah DD; Achmad SN; Wasito, 1989. Endoparasites and dermatitis in cattle in Tanah Laut, South Kalimantan. Penyakit Hewan, 33(37):55-58; 9 ref.
Tavasou M; Rahbari S, 1998. Sero-epidemiological Survey of Babesia ovis in sheep at different geographical regions of Iran. Journal of the Faculty Veterinary Medicine, University of Tehran, 53(3-4):55-550.
Thomford JW; Conrad PA; Boyce WM; Holman PJ; Jessup DA, 1993. Isolation and in vitro cultivation of Babesia parasites from free-ranging desert bighorn sheep (Ovis canadensis nelsoni) and mule deer (Odocoileus hemionus) in California. Journal of Parasitology, 79(1):77-84; 21 ref.
Tjornchos K; Lawrences JA; Whiteland AP; Kafuwa PT, 1996. Field observations on the duration of immunity in cattle after vaccination against Anaplasma and Babesia species. Onderstepoort Journal of Veterinary Research, 63(1):1-5.
Tomassone L; Pagani P; De Meneghi D, 2005. Detection of Babesia caballi in Amblyomma variegatum ticks (Acari: Ixodidae) collected from cattle in the Republic of Guinea. Parassitologia, 47:247-51.
Trifonov T; Rusev V, 1989. Epizootiological study of piroplasmosis of cattle and sheep and its tick vectors in the Stranja region of Bulgaria. I. Piroplasmosis. Veterinarna Sbirka, 87(9):43-46; 7 ref.
Urquhart GM; Armour J; Duncan JL; Dunn AM; Jennings FW, 1996. Veterinary parasitology. Second edition. Oxford UK, Blackwell Science Ltd., pp. 307.
Van Andel JM; Dwinger RH; Alvarez JA, 1997. Study of Anaplasma and Babesia infection rates of cattle and associated ticks in the coast of Guatemala. Revue de Elevage et de Medicine Veterinary des Pays Tropicaux, 50(4):285-292.
Vargas E; Alvarez V; Herrero MV; Pérez E; Buening GM, 1997. Serological survey for Babesia bovis and Babesia bigemina infections among young cattle of a breeding herd in the dry tropical climate of Costa Rica. Ciencias Veterinarias (Heredia), 20(1/2):33-46; 36 ref.
Veit HP; McCarthy F; Friedericks J; Cashin M; Angert R, 1993. A survey of goat and cattle diseases in the Artibonite Valley, Haiti, West Indies. Revue d'élevage et de Médecine Vétérinaire des Pays Tropicaux, 46(1/2):27-38; [Actes de la 2e Réunion Biennale de la Society for Tropical Veterinary Medicine, 2-6 février 1992, Saint-FranÇois, Guadeloupe.]; 17 ref.
Vidotto O; Andrade GM; Amaral CHS; Barbosa CS; Freire RL; Rocha MA; Vidotto MC, 1997. Frequency of antibodies against Babesia bigemina, B. bovis and Anaplasma marginale in dairy herds in the Londrina region, Paraná State, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 49(5):655-659; 8 ref.
Vos AJde; Waal DTde; Jackson LA, 2004. Bovine babesiosis. In: Infectious diseases of livestock, Volume One, Ed.2 [ed. by Coetzer, J. A. W.\Tustin, R. C.]. Oxford, UK: Oxford University Press, 406-424.
Waldrup KA; Collisson E; Bentsen SE; Winkler CK; Wagner GG, 1989. Prevalence of erythrocytic protozoa and serologic reactivity to selected pathogens in deer in Texas. Preventive Veterinary Medicine, 7(1):49-58; 36 ref.
Weber C, 1988. Epidemiology of Babesia divergens infections in cattle in North Germany. 2. Immunization with live vaccine on three farms. Epidemiologie der Babesia divergens-Infektion bei Rindern in Norddeutschland. 2. Vakzinierung mit einer Lebendvakzine in drei Beständen., 140 pp.; 125 ref.
Western KA; Benson GD; Gleason NN; Healy GR; Shultz MG, 1970. Babesiosis in a Massachusetts resident. N. Engl. J. Med., 283:854-856.
Wright IG; Kerr JD, 1977. Hypotension in acute Babesia bovis (=B. argentina) infections in splenectomised calves. Journal of Comparative Pathology, 87:531-537.
Yeruham I; Hadani A; Galker F; Rosen S, 1989. Notes on the biology of the tick Rhipicephalus bursa (Canestrini and Fanzago, 1877) in Israel. Revue d'élevage et de Médecine Vétérinaire des Pays Tropicaux, 42(2):233-235; 16 ref.
Zintl A; Gray JS; Skerrett HE; Mulcahy G, 2005. Possible mechanisms underlying age-related resistance to bovine babesiosis. Parasite Immunology, 27:115-20.
Zintl A; Mulcahy G; Skerrett HE; Taylor SM; Gray JS, 2003. Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clinical Microbiology Reviews, 16:622-36.
Zintl A; Westbrook C; Skerrett HE; Gray JS; Mulcahy G, 2002. Chymotrypsin and neuraminidase treatment inhibits host cell invasion by Babesia divergens (Phylum Apicomplexa). Parasitology, 125(1):45-50; 15 ref.
Zintz R, 1990. Epidemiology of blood parasitic infections on milk-producing farms in Valle and Quindio (Colombia). Untersuchungen zur Epidemiologie der Hämoparasitosen in milchproduzierenden Betrieben in Valle und Quindio (Kolumbien)., 131 pp.; 15 pp. of ref.
Abo-Shehada M N, Muwalla M M, Tawfeek F, 1988. Ovine babesiosis in Jordanian sheep mistakenly diagnosed as plant poisoning. Preventive Veterinary Medicine. 6 (3), 235-238. DOI:10.1016/0167-5877(88)90033-5
Aguirre D H, Bermúdez A C, Mangold A J, Guglielmone A A, 1990. Natural infections with Babesia bovis and Babesia bigemina in Hereford, Criolla and Nelore cattle in Tucumán, Argentina. (Infección natural con Babesia bovis y Babesia bigemina en bovinos de raza Hereford, Criolla y Nelore en Tucumán, Argentina.). Revista de Medicina Veterinaria (Buenos Aires). 71 (2), 54-60.
Alani A J, Herbert I V, 1988. The morphometrics of Babesia motasi (Wales) and its transmission by Haemaphysalis punctata (Canestrini and Fanzago 1877) to sheep. Veterinary Parasitology. 30 (2), 87-95. DOI:10.1016/0304-4017(88)90155-0
Alonso M, Camus E, Rodriguez Diego J, Bertaudière L, Tatareau J C, Liabeuf J M, 1992. Current position of bovine haemoparasitoses in Martinique (French West Indies). (Situation actuelle des hémoparasitoses bovines en Martinique (Antilles françaises).). Revue d'Élevage et de Médecine Vétérinaire des Pays Tropicaux. 45 (1), 9-14.
Alvarez V, Herrero M V, 1996. A bibliographic review of Boophilus microplus (Acari: Ixodidae) and the diseases it transmits in Costa Rica. (Bibliografia sobre Boophilus microplus (Acari: Ixodidae) y enfermedades transmitidas por esta en Costa Rica.). Ciencias Veterinarias (Heredia). 19 (1/2), 1-9.
Arai S, Tsuji M, Kim SamJu, Nakada K, Kirisawa R, Ohta M, Ishihara C, 1998. Antigenic and genetic diversities of Babesia ovata in persistently infected cattle. Journal of Veterinary Medical Science. 60 (12), 1321-1327.
Ashmawy K E, El-Wafa S A A, Fadly R S, 1998. Incidence of Babesia bigemina infection in native breed cattle, Behera Province, Egypt using different methods of diagnosis. Assiut Veterinary Medical Journal. 39 (77), 110-120.
Bai Q, Liu G Y, Zhang L, Zhou J Y, 1990. Studies on the isolation and preservation of a single species of bovine haematocytozoon: the finding and isolation of Babesia ovata in China. Chinese Journal of Veterinary Medicine. 16 (12), 2-4.
Barbosa M F R, Costa J O, Tafuri W L, 1994. Congenital transmission of Babesia bovis: first autochthonous case in Minas Gerais, Brazil. (Transmissão congênita de Babesia bovis: relato de um caso autóctone em Minas Gerais - Brasil.). Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 46 (5), 519-526.
Barci L A G, Oliveira M R, Machado R Z, Oliveira D A, Araújo Filho R S, 1994. Epidemiology of cattle babesiosis in the São Paulo State: I. Studies in dairy cattle of type B from Pindamonhagaba county, Paraiba Valley. (Epidemiologia da babesiose bovina no estado de São Paulo: I. Estudo em rebanhos produtores de leite tipo B do município de pindamonhangaba, Vale do Paraíba.). Revista Brasileira de Parasitologia Veterinária. 3 (2), 79-82.
Barré N, 1997. The ticks of ruminants of the Lesser Antilles: their biology, their economic importance and defensive strategies. (Les tiques des ruminants dans les Petites Antilles: biologie, importance économique, principes de lutte.). Productions Animales. 10 (1), 111-119.
Basalo A R, Parra O, Arraga de Alvarado C M, León E, Guillén A, 1995. Establishment of the indirect immunofluorescence serological technique as a diagnostic method for bovine babesiosis in the diagnostic laboratory of the veterinary clinic at the University of Zulia. (Establecimiento de la técnica serológica de inmunofluorescencia indirecta (I.F.I.) como método de diagnóstico de la babesiosis bovina en el laboratorio de diagnóstico de la policlínica veterinaria de L.U.Z.). Revista Cientifica, Facultad de Ciencias Veterinarias, Universidad del Zulia. 5 (2), 87-94.
Ben Said M S, 1993. Babesiasis of goats in northern Tunisia. Epidemiological and clinical observations. (La babésiose caprine dans le nord de la Tunisie - observations épidémio-cliniques.). Etudes et Synthèses de l'IEMVT. 664-682.
Bossche P van den, Mudenge D, 1999. The effect of short-interval deltamethrin applications to control tsetse on the seroprevalence of babesiosis in cattle. Tropical Animal Health and Production. 31 (4), 215-222. DOI:10.1023/A:1005215126760
Brun-Hansen H, Christensson D A, Eide D M, Grønstol H, 1998. Experimental infection with Babesia divergens in cattle persistently infected with bovine virus diarrhoea virus. Journal of Veterinary Medicine. Series B. 45 (5), 269-277. DOI:10.1111/j.1439-0450.1998.tb00794.x
CABI, Undated. Compendium record. Wallingford, UK: CABI
CABI, Undated a. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI
Camus E, Montenegro-James S, 1994. Bovine anaplasmosis and babesiosis in the Lesser Antilles: risk assessment of an unstable epidemiologic situation. In: Veterinary Research [International Symposium on ecopathology and animal health management, Clermont-Ferrand, 18-20 October 1993.], 25 (2/3) 313-317.
Cardozo H, Solari M A, Etchebarne J, Larrauri J H, 1994. Seroepidemiological study of Babesia bovis in support of the Uruguayan Boophilus microplus control program. Revista Brasileira de Parasitologia Veterinária. 3 (1), 5-8.
Carrique Mas J J, Widdowson M A, Cuéllar A M, Ribera H, Walker A R, 2000. Risk of babesiosis and anaplasmosis in different ecological zones of Santa Cruz Department, Bolivia. Veterinary Parasitology. 93 (1), 29-38. DOI:10.1016/S0304-4017(00)00328-9
Dreyer K, Fourie L J, Kok D J, 1998. Epidemiology of tick-borne diseases of cattle in Botshabelo and Thaba Nchu in the Free State Province. Onderstepoort Journal of Veterinary Research. 65 (4), 285-289.
Egbe-Nwiyi T N, Chaudhari S U R, 1996. Haematological studies on haemoparasites of different breeds of cattle in arid zone of north-eastern Nigeria: preliminary observations. Pakistan Veterinary Journal. 16 (3), 149-151.
El-Seify M A, Eissa N A, 1990. Some clinico-pathological studies on cattle naturally infected with blood parasites in Beni-Suef Governorate. Egyptian Journal of Comparative Pathology and Clinical Pathology. 3 (1), 37-43.
Fadraga M, Cordovés C O, Puentes T, 1991. Circulation of antibodies to haemoparasites in cattle (Bos taurus) of high genetic value in Cuba. (Circulación de anticuerpos de hemoparásitos en ganado (Bos taurus) de alto valor genético en la República de Cuba.). Revista Cubana de Ciencias Veterinarias. 22 (3), 249-255.
Figueroa J V, Alvarez J A, Ramos J A, Rojas E E, Santiago C, Mosqueda J J, Vega C A, Buening G M, 1998. Bovine babesiosis and anaplasmosis follow-up on cattle relocated in an endemic area for hemoparasitic diseases. In: Annals of the New York Academy of Sciences [Tropical veterinary medicine: molecular epidemiology, hemoparasites and their vectors, and general topics.], 849 [ed. by Jongejan F, Goff W, Camus E]. 1-10. DOI:10.1111/j.1749-6632.1998.tb11027.x
Flach E J, Shambwana I A, Dolan T T, Kassim A, Pedersen H, Glass M, Morzaria S P, 1989. East Coast fever immunization trials on Unguja Island, Zanzibar. In: Theileriosis in eastern, central and southern Africa. Proceedings of a workshop on East Coast fever immunization held in Lilongwe, Malawi 20-22 September 1988 [Theileriosis in eastern, central and southern Africa. Proceedings of a workshop on East Coast fever immunization held in Lilongwe, Malawi 20-22 September 1988], [ed. by Dolan TT]. Nairobi, Kenya: International Laboratory for Research on Animal Diseases. 77-82.
Freidhoff KT, Ganse-Dumrath D, Weber C, Dumrath DG, 1988. Epidemiology and prophylaxis of babesiosis (Babesia divergens) in cattle. In: Symposium "Weideparasitosen Bad Zwischenahn, 17 und 18 September 1987, Kurz fassung der Vortrage, 52-56.
Gaido A B, Aguirre D H, Echaide S T de, Guglielmone A A, 1997. Clinical incidence of primary Babesia bovis infections in dairy cattle in the Lerma Valley, Province of Salta, Argentina. (Incidencia clínica de infecciones primarias por Babesia bovis en bovinos lecheros del Valle de Lerma, Provincia de Salta.). Veterinaria Argentina. 14 (137), 460-463.
García Cuadrado N, 1993. Sanitary aspects of beef cattle farming: parasitoses. (Aspectos sanitarios de la explotación de vacuno de carne: parasitosis.). In: Vacuno de carne en extensivo. Curso celebrado en el Servicio de Investigacion y Desarrollo Tecnologico de Extramadura del 19 al 30 de noviembre de 1991. [ed. by Lopez de Torre G (Coordinator)]. Mérida, Spain: Junta de Extremadura. 303-330.
Gern L, Kindler A, Brossard M, 1988. Annual evolution of cattle immunity against Babesia divergens in northern Switzerland. Preventive Veterinary Medicine. 6 (1), 9-16. DOI:10.1016/0167-5877(88)90021-9
Gitau G K, Perry B D, Katende J M, McDermott J J, Morzaria S P, Young A S, 1997. The prevalence of serum antibodies to tick-borne infections in cattle in smallholder dairy farms in Murang'a District, Kenya; a cross-sectional study. Preventive Veterinary Medicine. 30 (2), 95-107. DOI:10.1016/S0167-5877(96)01100-2
Gräfner G, 1989. Present distribution, importance and control of parasitoses of grazing cattle in the GDR. (Zur derzeitigen Verbreitung, Bedeutung und Bekämpfung der Weideparasitosen des Rindes in der DDR.). Monatshefte für Veterinärmedizin. 44 (13), 435-437.
Gray J S, Murphy T M, Taylor S M, Blewett D A, Harrington R, 1990. Comparative morphological and cross transmission studies with bovine and deer babesias in Ireland. Preventive Veterinary Medicine. 9 (3), 185-193. DOI:10.1016/0167-5877(90)90065-P
Guglielmone A A, Aguirre D H, Späth E J A, Gaido A B, Mangold A J, Ríos L G de, 1992. Long-term study of incidence and financial loss due to cattle babesiosis in an Argentinian dairy farm. Preventive Veterinary Medicine. 12 (3-4), 307-312. DOI:10.1016/0167-5877(92)90058-N
Guglielmone A A, Lugaresi C I, Volpogni M M, Anziani O S, Vanzini V R, 1997. Babesial antibody dynamics after cattle immunisation with live vaccines, measured with an indirect immunofluorescence test. Veterinary Parasitology. 70 (1/3), 33-39. DOI:10.1016/S0304-4017(96)01143-0
Ha Thuy Hanh, Nguyen Dang Khai, Pham Sy Lang, Phan Dich Lan, Nguyen Duc Tan, Hoang Manh Lam, 1997. Blood parasites of cattle in Daklak province, Vietnam. (Mot so nhan xet ve tinh hinh nhiem cac bao tu trung mau (haemosporidia) o bo tinh Dac Lac.). Khoa Hoc Ky Thuat Thu Y. 4 (4), 50-53.
Hadot under˜ Thúy Hadot under˜nh, Nguyên Dăng Khǡi, Phan Didot under˜ch Lân, Phadot under˜m Sy˜ Lăng, 1996. Observations on hemosporidian infections in dairy cattle in the Hanoi area. (Môdot under˜t sôacute˜ nhâdot under˜n xét tình hính nhiê˜m huyêacute˜t bào tu trùng o bò su˜a vùng ngoadot under˜i vi Hà Nôdot under˜i.). Khoa Hoc Ky Thuat Thu Y. 3 (2), 61-64.
Hardeng F, 1991. Epidemiology of diseases transmitted by ticks. A review with special emphasis on diseases transmitted by Ixodes ricinus in ruminants in Norway. (Epidemiologiske forhold ved flåttbårne sjukdommer. En oversikt med spesiell vekt på sjukdommer overført av Ixodes ricinas hos drøvtyggere i Norge.). Norsk Veterinærtidsskrift. 103 (10), 913-921.
Hugh JME, Scotland K, Applewhaite LM, Alexander FM, 1988. Seroprevalence of anaplasmosis and babesiosis in livestock on St. Lucia, 1983. In: Tropical Animal Health and Production, 20 137-139.
Jongejan F, Perry B D, Moorhouse P D S, Musisi F L, Pegram R G, Snacken M, 1988. Epidemiology of bovine babesiosis and anaplasmosis in Zambia. Tropical Animal Health and Production. 20 (4), 234-242. DOI:10.1007/BF02239989
Jorgensen W K, Weilgama D J, Navaratne M, Dalgliesh R J, 1992. Prevalence of Babesia bovis and Anaplasma marginale at selected localities in Sri Lanka. Tropical Animal Health and Production. 24 (1), 9-14. DOI:10.1007/BF02357227
Jorgensen W, Weilgama D J, Navaratne M, Weerasinghe C, Perera P S G, 1988. Observations on the prevalence of Babesia and Anaplasma infections in some Government livestock farms in Sri Lanka. In: Sri Lanka Veterinary Journal, 36 56-57.
Kabagambe J, Nshimiyimana A, Muberuka J, Nyiligira J B, 1988. The enzootic diseases of cattle at Bugesera. (Lés maladies enzootiques des bovins au Bugesera.). Bulletin Agricole du Rwanda. 21 (3), 159-168.
Kang Y B, Jang H, 1988. Parasitaemia induced by splenectomy in a calf naturally infected with Theileria sergenti and Babesia ovata. Research Reports of the Rural Development Administration, Veterinary, Korea Republic. 30 (2), 7-11.
Katsande TC, More SJ, Bock RE, Mabikacheche L, Molloy JB, Ncobe C, 1999. A Serological survey of bovine babesiosis in Northern and Eastern Zimbabwe. In: Ondersterpoort Journal of Veterinary Research, 66 (4) 255-263.
Kjemtrup A M, Thomford J W, Gardner I A, Conrad P A, Jessup D A, Boyce W M, 1995. Seroprevalence of two Babesia spp. isolates in selected bighorn sheep (Ovis canadensis) and mule deer (Odocoileus hemionus) populations in California. Journal of Wildlife Diseases. 31 (4), 467-471.
Koch H T, Kambeva L, Ocama J G R, Munatswa F C, Franssen F F J, Uilenberg G, Dolan T T, Norval R A I, 1990. Immunization of cattle against Theileria parva bovis and their exposure to natural challenge. Veterinary Parasitology. 37 (3-4), 185-196. DOI:10.1016/0304-4017(90)90002-S
Komoin-Oka C, Zinsstag J, Pandey V S, Fofana F, N'Depo A, 1999. Epidemiology of parasites of sheep in the southern forest zone of Côte d'Ivoire. (Epidémiologie des parasites des ovins de la zone sud forestière de la Côte d'Ivoire.). Revue d'Élevage et de Médecine Vétérinaire des Pays Tropicaux. 52 (1), 39-46.
Lawrence J A, Musisi F L, Mfitilodze M W, Tjornehoj K, Whiteland A P, Kafuwa P T, Chamambala K E, 1996. Integrated tick and tick-borne disease control trials in crossbred dairy cattle in Malawi. Tropical Animal Health and Production. 28 (4), 280-288. DOI:10.1007/BF02240818
Lew A E, Bock R E, Croft J M, Minchin C M, Kingston T G, Dalgliesh R J, 1997. Genotypic diversity in field isolates of Babesia bovis from cattle with babesiosis after vaccination. Australian Veterinary Journal. 75 (8), 575-578. DOI:10.1111/j.1751-0813.1997.tb14197.x
Linhares G F C, Massard C L, Araujo J L de B, Alves L C, 1992. Serological survey of Babesia bigemina (Smith & Kilborne, 1893) and Babesia bovis (Babés, 1888) in cattle from the central western region of Brazil. (Levantamento sorológico para Babesia bigemina (Smith & Kilborne, 1893) e Babesia bovis (Babés, 1888) em bovinos na região centro-oeste do Brasil.). Arquivos da Universidade Federal Rural do Rio de Janeiro. 15 (1), 85-91.
Liu ZhongLing, Zhao JunLong, Ma LiHua, Yao BoaAn, 1997. Studies on buffalo babesiosis in Hubei province, China. In: Tropical Animal Health and Production [Proceedings of the European Union International Symposium on ticks and tickborne diseases, September 2-6, 1996, Xi'an, China.], 29 (4 (supplement)) [ed. by Preston P M, Yin Hong]. 33S-36S.
Lonneux J F, Losson B, Collin B, 1991. Specific Babesia antibodies in deer in the South of Belgium. (Anticorps spécifiques contre Babesia, chez les cervidés du Sud de la Belgique.). Annales de Médecine Vétérinaire. 135 (2), 119-121.
Losson B, 1989. Babesia infection of cattle in Belgium: results of an enquiry among veterinarians. (La babésiose bovine en Belgique:à propos d'une enquête auprès des vétérinaires.). Annales de Médecine Vétérinaire. 133 (1), 63-67.
Losson B, Lefevre F, 1989. Bovine babesiosis in Belgium. A serological survey in an endemic zone. (La babésiose bovine en Belgique. Une enquête sérologique en zone d'endémie.). Annales de Médecine Vétérinaire. 133 (5), 421-426.
Lu W S, Yin H, Lu W X, Yu F, Zhang Q C, Dou H F, 1988. Discovery of Babesia major in cattle and confirmation of its transmitting vector tick in China. Chinese Journal of Veterinary Science and Technology. 11-14.
Lu W S, Yin H, Lu W X, Zhang Q C, Yu F, Dou H F, 1990. Experimental studies on transovarian transmission of Babesia major from bovines by the tick Haemaphysalis longicornis. Chinese Journal of Veterinary Science and Technology. 5-6.
Lu WenXiang, Lu WanShun, Zhang QiCai, Luo JianXun, Yin Hong, Dou HuiFang, 1995. Survey of the species of tick-transmitted haemocytozoa of cattle and the distribution features in China. Chinese Journal of Veterinary Science and Technology. 25 (8), 13-16.
Ma L H, Liu Z L, Zao J L, 1989. An investigation of babesiosis in buffaloes in Hubei Province. 5. The experimental demonstration of the transovarian transmission of Babesia bovis by Rhipicephalus haemaphysaloides haemaphysaloides. Acta Veterinaria et Zootechnica Sinica. 20 (1), 67-70.
Madruga C R, Suarez C E, McElwain T F, Palmer G H, 1996. Conservation of merozoite membrane and apical complex B cell epitopes among Babesia bigemina and Babesia bovis strains isolated in Brazil. Veterinary Parasitology. 61 (1/2), 21-30. DOI:10.1016/0304-4017(95)00809-8
Madruga CR, Braga MM, Oliveira DB, Massard CL, Soares CO, Oliveira DB, 2000. Prevalence of antibodoes against Babesia bovis (Babes 1888) and B. bigemina (Smith and Kilborne, 1893) (Apicomlexa:Babesiidae) in cattle from four municipalities of Rio de Janeiro State. In: Revista Brasileira de Ciencias Veterinaria, 7 (2) 113-116.
Majaj-Büscher H, 1992. Ectoparasites and blood parasites of goats in Jordan. (Untersuchungen zum Befall von Ziegen mit Ektoparasiten und Blutparasiten in Jordanien.). Germany: Fachbereich Veterinärmedizin, Freie Universität, Berlin. 119 pp.
Marín J, Rol J A, Navarrete I, Habela M A, 1995. Serological survey of babesiosis in sheep in the province of Badajoz, Spain. (Aportaciones al conocimiento epidemiológico de la babesiosis ovina (Babesia ovis) en la provincia de Badajoz. Seroprevalencia y transmisión experimental por ixódidos.). Medicina Veterinaria. 12 (7/8), 460...470.
Martin T, Epstoin V, 1999. The animal health status of the Solomon Islands, 1991., 34 pp.
Molloy J B, Bowles P M, Bock R E, Turton J A, Katsande T C, Katende J M, Mabikacheche L G, Waldron S J, Blight G W, Dalgliesh R J, 1998. Evaluation of an ELISA for detection of antibodies to Babesia bovis in cattle in Australia and Zimbabwe. Preventive Veterinary Medicine. 33 (1/4), 59-67. DOI:10.1016/S0167-5877(97)00063-9
Mota R A, Soares P C, Silva F, Soares C O, Lopes C W G, Massard C L, 2000. Babesiosis in goat on Pernambuco State, Brazil. (Babesiose caprina no estado de pernambuco, Brasil.). Revista Brasileira de Medicina Veterinária. 22 (2), 78-80.
Mulei C M, Rege J E O, 1989. An examination of the incidences of East Coast Fever (ECF), anaplasmosis, and babesiosis in the bovine in Kabete area of Kiambu District of Kenya. Bulletin of Animal Health and Production in Africa. 37 (3), 213-216.
Munatswa FC, Dolan TT, 1989. Theileriosis in Zimbabwe. [Proceedings of a workshop on East coast fever immunization held in Lilongwe, Malawi, 20-22 September, 1988], ILRAD.
Musisi F L, Quiroga J C, Ngulube B, Kanhai G K, 1989. An East Coast fever immunization field trial at Kasoba, Malawi. In: Theileriosis in eastern, central and southern Africa. Proceedings of a workshop on East Coast fever immunization held in Lilongwe, Malawi 20-22 September 1988 [Theileriosis in eastern, central and southern Africa. Proceedings of a workshop on East Coast fever immunization held in Lilongwe, Malawi 20-22 September 1988], [ed. by Dolan T T]. Nairobi, Kenya: International Laboratory for Research on Animal Diseases. 71-76.
Nari A, Solari M A, 1991. Distribution and control of Boophilus microplus in Uruguay, and their relation with Babesia spp. (Epidemiología y control del Boophilus microplus en Uruguay. Su relación con Babesia spp.). Revista Cubana de Ciencias Veterinarias. 22 (3), 149-160.
Nevils M A, Figueroa J V, Turk J R, Canto G J, Le V, Ellersieck M R, Carson C A, 2000. Cloned lines of Babesia bovis differ in their ability to induce cerebral babesiosis in cattle. Parasitology Research. 86 (6), 437-443. DOI:10.1007/s004360050691
Nguyen Van Hau, Nhu Van Thu, Ha Thuy Hanh, Le Minh Sat, 1999. A preliminary study on application of polymerase chain reaction in diagnosis of haemosporidiosis in cattle. Khoa Hoc Ky Thuat Thu Y (Veterinary Sciences and Techniques). 6 (1), 48-52.
Niepold J, 1990. Examination of cattle sera for simultaneous infection with Borrelia burgdorferi and Babesia divergens. (Untersuchung von Rinderseren auf das simultane Vorkommen von Infektionen mit Borrelien (Borrelia burgdorferi) und Babesien (Babesia divergens).). Germany: Tierärztliche Hochschule Hannover, Hannover. 89 pp.
Nierlich S, 1990. An ELISA for the serodiagnosis of Babesia ovis in sheep. (Ein ELISA zur Serodiagnose von Babesia ovis-Infektion beim Schaf.). Germany: Tiërztliche Hochschule Hannover, Hannover. 144 pp.
Nowak F, 1990. Epidemiological investigation of cattle herds in central Sinutal, Cordoba province, Colombia. (Epidemiologische Untersuchungen in Rinderbeständen im mittleren Sinutal (Cordoba, Kolumbien).). German Federal Republic: Tierärztliche Hochschule, Hannover. 102 pp.
Ohta M, Kawazu S, Tsuji N, Terada Y, Kamio T, Fujisaki K, 1995. Rapid and sensitive method for detection of newly isolated Babesia parasite (Babesia sp. 1) in the anticipated vector-tick using the polymerase chain reaction technique. Journal of Protozoology Research. 5 (3), 108-117.
OIE Handistatus, 2005. World Animal Health Publication and Handistatus II (dataset for 2004)., Paris, France: Office International des Epizooties.
OIE, 2009. World Animal Health Information Database - Version: 1.4., Paris, France: World Organisation for Animal Health. https://www.oie.int/
OIE, 2012. World Animal Health Information Database. Version 2., Paris, France: World Organisation for Animal Health. https://www.oie.int/wahis_2/public/wahid.php/Wahidhome/Home
Pangui L J, Salifou S, 1992. Parasitological studies of tickborne haemoparasites in livestock in Benin. (Enquêtes parasitologiques sur les hémoparasites des bovins transmis par les tiques au Bénin.). World Animal Review. 73 (4), 48-50.
Papadopoulos B, Brossard M, Perié N M, 1996a. Piroplasms of domestic animals in the Macedonia region of Greece; 2. Piroplasms of cattle. Veterinary Parasitology. 63 (1/2), 57-66. DOI:10.1016/0304-4017(95)00845-4
Papadopoulos B, Brossard M, Perié N M, 1996b. Piroplasms of domestic animals in the Macedonia region of Greece. 3. Piroplasms of small ruminants. Veterinary Parasitology. 63 (1/2), 67-74. DOI:10.1016/0304-4017(95)00846-2
Papadopoulos B, Perié N M, Uilenberg G, 1996. Piroplasms of domestic animals in the Macedonia region of Greece. 1. Serological cross-reactions. Veterinary Parasitology. 63 (1/2), 41-56. DOI:10.1016/0304-4017(95)00878-0
Payne R C, Osorio O, 1990. Tick-borne diseases of cattle in Paraguay. I. Seroepidemiological studies on anaplasmosis and babesiosis. Tropical Animal Health and Production. 22 (1), 53-60. DOI:10.1007/BF02243500
Perez E, Herrero M V, Jimenez C, Carpenter T E, Buening G B, 1994. Epidemiology of bovine anaplasmosis and babesiosis in Costa Rica. Preventive Veterinary Medicine. 20 (1/2), 23-31. DOI:10.1016/0167-5877(94)90105-8
Pino R, Salabarría F F, 1989. Prevalence of Babesia bigemina (Smith & Kilborne 1983) during the period January-May 1987 in the Provinces of Ciudad de la Habana and La Habana. (Prevalencia de Babesia bigemina (Smith y Kilborne, 1983) en el período enero-mayo de 1987 en las provincias de Ciudad de la Habana y La Habana.). Revista Cubana de Ciencias Veterinarias. 20 (4), 227-232.
Prosperi S, Baldelli R, Fioravanti M L, Roda R, Galuppi R, Michelini S, 1990. Pasture and bovine health risks. II. Serological survey for brucellosis, Q fever, chlamydiosis and babesiosis. (Pascolo e rischi sanitari per il bovino. Nota II: indagine sierologica per brucellosi, febbre Q, clamidiosi e babesiosi.). Obiettivi e Documenti Veterinari. 59-61.
Purnell R E, Gunter T D, Schröder J, 1989. Development of a prophylactic regime using long-acting tetracycline for the control of redwater and heartwater in susceptible cattle moved into an endemic area. Tropical Animal Health and Production. 21 (1), 11-19. DOI:10.1007/BF02297335
Quijada T, Contreras J, Foriano M, 1998. Babesia bigemina seropositivity in crossbred cattle from Las Yaguas, Lara State, Venezuela. (Seropositividad a Babesia bigemina en bovinos mestizos de Las Yaguas, estado Lara, Venezuela.). Veterinaria Tropical. 23 (1), 13-24.
Ribera Cuéllar H, Cuéllar A M, Barba Chávez G, Carrique-Mas J J, Walker A, 2000. Study of babesiosis and anaplasmosis in relation to tick burdens of dairy calves in the eastern Bolivian lowlands. (Estudio sobre babesiosis y anaplasmosis en relación con la carga de garrapatas en terneros lecheros del oriente boliviano.). Veterinaria México. 31 (1), 39-46.
Rodriguez O N, Rodriguez P, Espaine L, Rivas A, 1989. Frequency of haemoparasites in sheep in Cuba. (Incidencia de hemoparásitos en los ovinos de Cuba.). Revista Cubana de Ciencias Veterinarias. 20 (1), 57-70.
Rosignoli C, Nigrelli A D, Savini G, Semproni G, Benaglia F, Franzini G, 2000. An outbreak of babesiosis (Babesia bovis) in a beef cattle fattening unit. (Episodio di babesiosi (Babesia bovis) in un allevamento di bovini de carne.). Obiettivi e Documenti Veterinari. 21 (3), 65-70.
Salem G H, 1999. Diagnosis of both Babesia bovis and Babesia bigemina infections among carrier cattle by using extra-chromosomal DNA-based polymerase chain reaction test in Egypt. Assiut Veterinary Medical Journal. 42 (83), 38-54.
Serra-Freire N M da, Nuernberg S, 1995. The cattle tick and babesiosis-anaplasmosis in Santa Catarina State, Brazil. (O carrapato e a tristeza parasitária bovina no Estado de Santa Catarina, Brasil.). Revista Brasileira de Medicina Veterinária. 17 (6), 257-259.
Shaw A A, 1989. Investigation on some infections in the exotic, pure and cross bred cattle of Kashmir valley. Indian Journal of Comparative Microbiology, Immunology and Infectious Diseases. 10 (1), 33-38.
Simoes Campos D A, Chirinos Rodríguez A R, Martínez de Chirinos N S, Castejón O, Avila J P, 1995. Prevalence of bovine babesiosis in Sector Cuatro (Playa Bonita), Mara county. (Prevalencia de babesiosis bovina en el Sector Cuatro (Playa Bonita) del municipio Mara.). Revista Cientifica, Facultad de Ciencias Veterinarias, Universidad del Zulia. 5 (1), 5-10.
Siswansyah D D, 1990. Prevalence of theileriosis, babesiosis and anaplasmosis in cattle and buffaloes in South Kalimantan. (Prevalensi theileriosis, babesiosis dan anaplasmosis pada sapi dan kerbau di Kalimantan Selatan.). Penyakit Hewan. 22 (39), 50-54.
Smeenk I, Kelly P J, Wray K, Musuka G, Trees A J, Jongejan F, 2000. Babesia bovis and B. bigemina DNA detected in cattle and ticks from Zimbabwe by polymerase chain reaction. Journal of the South African Veterinary Association. 71 (1), 21-24.
Soares C O, Souza J C P, Madruga C R, Madureira R C, Massard C L, Fonseca A H, 2000. Seroprevalence of Babesia bovis in cattle in the Norte Fluminense region. (Soroprevalência de Babesia bovis em bovinos na mesorregião Norte Fluminense.). Pesquisa Veterinária Brasileira. 20 (2), 75-79. DOI:10.1590/S0100-736X2000000200004
Solomon G, Kaaya G P, Gebreab F, Gemetchu T, Tilahun G, 1998. Ticks and tick-borne parasites associated with indigenous cattle in Didtuyura Ranch, southern Ethiopia. Insect Science and its Application. 18 (1), 59-66.
Solorio-Rivera J L, Rodríguez-Vivas R I, Pérez-Gutierrez E, Wagner G, 1999. Management factors associated with Babesia bovis seroprevalence in cattle from eastern Yucatán, Mexico. Preventive Veterinary Medicine. 40 (3/4), 261-269. DOI:10.1016/S0167-5877(99)00019-7
Tavasoli M, Rahbari S, 1998. Seroepidemiological survey of Babesia ovis in sheep at different geographical regions of Iran. Journal of the Faculty of Veterinary Medicine, University of Tehran. 53 (3/4), 55-59.
Thomford J W, Conrad P A, Boyce W M, Holman P J, Jessup D A, 1993. Isolation and in vitro cultivation of Babesia parasites from free-ranging desert bighorn sheep (Ovis canadensis nelsoni) and mule deer (Odocoileus hemionus) in California. Journal of Parasitology. 79 (1), 77-84. DOI:10.2307/3283281
Tjornehoj K, Lawrence J A, Whiteland A P, Kafuwa P T, 1996. Field observations on the duration of immunity in cattle after vaccination against Anaplasma and Babesia species. Onderstepoort Journal of Veterinary Research. 63 (1), 1-5.
Vargas E, Alvarez V, Herrero M V, Pérez E, Buening G M, 1997. Serological survey for Babesia bovis and Babesia bigemina infections among young cattle of a breeding herd in the dry tropical climate of Costa Rica. (Determinación de la incidencia a seropositividad, infección a Babesia bovis y Babesia bigemina (Hemosporidia: Babesiidae), en animales menores de un año, de una finca de cria, en un clima tropical seco de Costa Rica.). Ciencias Veterinarias (Heredia). 20 (1/2), 33-46.
Vidotto O, Andrade G M, Amaral C H S, Barbosa C S, Freire R L, Rocha M A, Vidotto M C, 1997. Frequency of antibodies against Babesia bigemina, B. bovis and Anaplasma marginale in dairy herds in the Londrina region, Paraná State, Brazil. (Freqüência de anticorpos contra Babesia bigemina, B. bovis e Anaplasma marginale em rebanhos leiteiros de região de Londrina, Paraná.). Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 49 (5), 655-659.
Waldrup K A, Collisson E, Bentsen S E, Winkler C K, Wagner G G, 1989. Prevalence of erythrocytic protozoa and serologic reactivity to selected pathogens in deer in Texas. Preventive Veterinary Medicine. 7 (1), 49-58. DOI:10.1016/0167-5877(89)90036-6
Weber C, 1988. Epidemiology of Babesia divergens infections in cattle in North Germany. 2. Immunization with live vaccine on three farms. (Epidemiologie der Babesia divergens-Infektion bei Rindern in Norddeutschland. 2. Vakzinierung mit einer Lebendvakzine in drei Beständen.). German Federal Republic: Tierärztliche Hochschule, Hannover. 140 pp.
Yeruham I, Hadani A, Galker F, Rosen S, 1989. Notes on the biology of the tick Rhipicephalus bursa (Canestrini and Fanzago, 1877) in Israel. Revue d'Élevage et de Médecine Vétérinaire des Pays Tropicaux. 42 (2), 233-235.
Yeruham I, Hadani A, Galker F, Rosen S, 1995. A study of an enzootic focus of sheep babesiosis (Babesia ovis, Babes, 1892). Veterinary Parasitology. 60 (3/4), 349-354. DOI:10.1016/0304-4017(95)00783-7
Zintz R, 1990. Epidemiology of blood parasitic infections on milk-producing farms in Valle and Quindio (Colombia). (Untersuchungen zur Epidemiologie der Hämoparasitosen in milchproduzierenden Betrieben in Valle und Quindio (Kolumbien).). Germany: Tierärztliche Hochschule Hannover, Hannover. 131 pp.
Zips S G, 1989. An epidemiological survey of Babesia bovis infections in Cordoba, Colombia. (Epidemiologische Untersuchung der Babesia bovis-Infektion in Cordoba (Kolumbien).). Germany: Tierärztliche Hochschule, Hannover. 112 pp.
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