Theileria annulata infections
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Theileria annulata infections
International Common Names
- English: Egyptian fever; Mediterranean Coast fever; theileriosis in ruminants - exotic; theileriosis, tropical; tropical theileriosis
- French: theileriose bovine d'Afrique du Nord
- Chinese: huan xing tai le chong bing
Local Common Names
- India: chichri rog
- Tunisia: boussofie
OverviewTop of page
Theileria annulata is a tickborne intracellular protozoan parasite of cattle, which occurs in North Africa, southern Europe, the Near and Middle East, India, China and Central Asia. It causes both mortality and reduced production, and has significant economic impacts as a result.
Datasheets are also available on bovine theilerioses and theileriosis in general (as well as other specific Theilieria infections).
Host AnimalsTop of page
|Animal name||Context||Life stage||System|
|Bos grunniens (yaks)||Domesticated host|
|Bos indicus (zebu)||Domesticated host||Cattle & Buffaloes: All Stages|
|Bos taurus (cattle)||Domesticated host||Cattle & Buffaloes: All Stages|
|Bubalus bubalis (Asian water buffalo)||Domesticated host||Cattle & Buffaloes: All Stages|
|Syncerus caffer||Wild host||Cattle & Buffaloes: All Stages|
Systems AffectedTop of page blood and circulatory system diseases of large ruminants
digestive diseases of large ruminants
mammary gland diseases of large ruminants
multisystemic diseases of large ruminants
nervous system diseases of large ruminants
reproductive diseases of large ruminants
respiratory diseases of large ruminants
skin and ocular diseases of large ruminants
urinary tract and renal diseases of large ruminants
DistributionTop of page
Updated information on the distribution of theileriosis in general (as distinct from Theileria annulata infections in particular) can be found in OIE's WAHID database on disease occurrence: http://www.oie.int/en/links/wahid/.
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Afghanistan||Present||Bulman et al., 1979|
|Armenia||Present||Marutyan, 1977; Marutyan, 1978; OIE, 1998|
|Azerbaijan||Present||, 1975; Askarov, 1975; Gumbatov and Bagirov, 1979; Stepanova et al., 1982; Movsum-Zade et al., 1983; OIE, 1998|
|Bangladesh||Present||Samad et al., 1983; Welte, 1994|
|-Anhui||Present||Song ShiRong, 1997|
|-Gansu||Present||Lu and Yin, 1994; Luo and Lu, 1997; Song ShiRong, 1997|
|-Hainan||Present||Song ShiRong, 1997|
|-Hebei||Present||Lu and Yin, 1994; Luo and Lu, 1997; Song ShiRong, 1997|
|-Heilongjiang||Present||Luo and Lu, 1997; Song ShiRong, 1997|
|-Henan||Present||Lu and Yin, 1994; Luo and Lu, 1997; Song ShiRong, 1997|
|-Hubei||Present||Lu and Yin, 1994; Luo and Lu, 1997; Song ShiRong, 1997|
|-Jilin||Present||Luo and Lu, 1997|
|-Liaoning||Present||Luo and Lu, 1997; Song ShiRong, 1997|
|-Nei Menggu||Present||Lu and Yin, 1994; Luo and Lu, 1997; Song ShiRong, 1997|
|-Ningxia||Present||Lu and Yin, 1994; Luo and Lu, 1997; Song ShiRong, 1997|
|-Shaanxi||Present||Lu and Yin, 1994; Luo and Lu, 1997|
|-Shandong||Present||Lu and Yin, 1994; Luo and Lu, 1997; Song ShiRong, 1997|
|-Shanxi||Present||Lu and Yin, 1994; Luo and Lu, 1997; Song ShiRong, 1997|
|-Xinjiang||Present||Lu and Yin, 1994; Guo et al., 1997; Luo and Lu, 1997; Song ShiRong, 1997|
|Georgia (Republic of)||Present||Matikashvili et al., 1978|
|-Andhra Pradesh||Widespread||Singh, 1991a; Sudhan et al., 1992|
|-Assam||Localised||Singh, 1991a; Sangwan, 2000|
|-Bihar||Widespread||Datta et al., 1988|
|-Chandigarh||Widespread||Beniwal et al., 1997|
|-Dadra and Nagar Haveli||Localised||Sangwan, 2000|
|-Delhi||Widespread||Beniwal et al., 1997; Sangwan, 2000|
|-Gujarat||Widespread||Singh, 1991a; Singh, 1991b; Singh, 1990|
|-Haryana||Widespread||, 1980; , 1982; Gautam et al., 1970; Gautam and Dhar, 1983; Yadav et al., 1985; Mallick et al., 1986; Sangwan et al., 1986; Sangwan, 2000|
|-Himachal Pradesh||Localised||Sharma et al., 1979; Jithendran, 1997; Sharma et al., 1999|
|-Indian Punjab||Present||Haque et al., 2010|
|-Jammu and Kashmir||Localised||Singh, 1991a; Shaw, 1989|
|-Karnataka||Widespread||Shastri et al., 1981; Shastri et al., 1993; Muraleedharan et al., 1994|
|-Madhya Pradesh||Widespread||Singh, 1991a; Sisodia and Mandial, 1986|
|-Maharashtra||Widespread||, 1981; Singh, 1991a; Shastri et al., 1993|
|-Odisha||Widespread||Singh, 1991a; Nayak and Dey, 1991; Sahoo and Misra, 1995|
|-Rajasthan||Widespread||, 1980; Singh, 1991a; Sharma et al., 1979; Tanwar et al., 1984|
|-Tamil Nadu||Widespread||Singh, 1991a; Anandan et al., 1983; Anandan and Lalitha, 1984; Venkataraman et al., 1984; Venkataraman and Manickam, 1992; Mukhopadhyay et al., 1997|
|-Uttar Pradesh||Widespread||Singh, 1991a; Mishra et al., 1989; Das and Sharma, 1991; Das, 1993; Mishra et al., 1994|
|-West Bengal||Widespread||Singh, 1991a; Bondopadhyay et al., 1992|
|Iran||Present||Rafyi and Maghami, 1962; Arshadi, 1976; Hooshmand-Rad, 1977; Hashemi-Fesharki, 1998; OIE, 1998|
|Iraq||Present||Khalifa and Kadhim, 1967; FAO, 1993; Arslan and Shukur, 1994|
|Israel||Present||Pipano, 1989a; Pipano, 1989b; Pipano, 1976; OIE, 1998|
|Kazakhstan||Present||Tutushin, 1979; Tutushin, 1981; Stepanova et al., 1982; Tutushin et al., 1982; Zablotsky, 1992; Sabanshiev, 1994|
|Kuwait||Present||Ahmed et al., 1987; FAO, 1997|
|Pakistan||Present||Khan and Huq, 1962; Zaki, 1965; Siddiqui, 1977; OIE, 1998; Muhammad et al., 1999|
|Saudi Arabia||Present||Hussein et al., 1991; Magzoub et al., 1992; Mottelib et al., 1992; El-Metenawy, 2000|
|Sri Lanka||Present||FAO, 1997|
|Syria||Present||Liebisch and Zukari, 1978; OIE, 1998|
|Tajikistan||Present||, 1983; Stepanova et al., 1982; Badalov, 1989; Vorob'eva, 1992; Zablotsky, 1992|
|Turkey||Present||Mimioglu, 1977; Sayin, 1991; OIE, 1998|
|Turkmenistan||Present||Khudainazarova, 1976; Zablotsky, 1992|
|United Arab Emirates||Present||OIE, 1998|
|Uzbekistan||Present||, 1983; Stepanova et al., 1982; Stepanova et al., 1986; Zablotsky, 1992; OIE, 1998|
|Algeria||Present||Sergent et al., 1945; Jore d'Arces, 1952; Rouina, 1984; Welte, 1994|
|Egypt||Present||Zaki, 1965; El-Refaii, 1977; Abd-El-Salam et al., 1994; OIE, 1998|
|Libya||Present||Norval et al., 1992|
|Mauritania||Present||Jacquiet et al., 1990; Jacquiet et al., 1994; D'Oliveira et al., 1995; D'Oliveira et al., 1997|
|Morocco||Present||Flach et al., 1995; Kachani et al., 1997; OIE, 1998|
|Sudan||Present||Mekki Osman, 1976; Shommein, 1977; Um El Hassan et al., 1983; Walker et al., 1983; OIE, 1998|
|Tunisia||Present||El and Sornicle, 1962; Dargouth et al., 1993; Ben Miled, 1994; Bahri et al., 1995; Darghouth et al., 1999|
|Bulgaria||Present||Pavlov, 1949; Pavlov, 1957|
|Greece||Present||Cardassis, 1964; Cardassis and Margaritis, 1964; Papadopoulos et al., 1996; Papadopoulos, 1999|
|Italy||Present||, 1999; Maxia et al., 1999|
|Macedonia||Present||Pavlov, 1949; Mikacic, 1952; Pavlov, 1957; FAO, 1997; OIE, 1998|
|Malta||Present||FAO, 1997; OIE, 1998|
|Moldova||Present||FAO, 1997; OIE, 1998|
|Portugal||Present||Leitao, 1943; OIE, 1998; Caeiro, 1999|
|Romania||Present||FAO, 1997; OIE, 1998|
|Russian Federation||Present||Present based on regional distribution.|
|-Russia (Europe)||Present||OIE, 1998|
|Spain||Present||, 1999; Viseras et al., 1997; OIE, 1998; Viseras and Garcia-Fernandez, 1999|
|Yugoslavia (former)||Present||Angelovski and Iliev, 1977; FAO, 1995|
PathologyTop of page
The chief pathological features of acute lethal tropical theileriosis are associated with dysfunction of the lymphoid and reticulo-endothelial system, and haematological changes (Dschunkowsky and Luhs, 1904; Neitz, 1957; Pipano, 1974, 1994; Levine, 1985). The general post-mortem findings (Figures 35-41) are as follows:
Carcasses: emaciated; anaemic; icteric; yellowish and gelatinous connective tissues.
Blood: appears watery.
Subcutaneous tissues: numerous petechial or larger haemorrhages.
Mucous membranes (pharynx, larynx, trachea, bronchi): pale; numerous petechial or haemorrhages.
Serous membranes: pale with numerous petechial or larger haemorrhages.
Lymph nodes: are markedly enlarged, oedematous, have varying degrees of haemorrhage, are frequently hyperplastic and hyperaemic.
Thymus: mildly congested.
Heart: myocardial muscular degeneration, petechial and ecchymotic haemorrhages of the epi- and endocardium.
Lungs: frequently oedematous and congested.
Spleen: splenomegaly due to lymphoid hyperplasia, spleen is soft and may have prominent malpighian corpuscles.
Liver: hepatomegaly; pale brown or yellow, friable, with evident parenchymatous degeneration.
Gall bladder: often markedly distended, produces dark-green viscid bile.
Kidneys: pale and congested, pseudoinfarcts of lymphoproliferative foci.
Adrenal glands: cortical haemorrhages, severely infiltrated.
Abomasum, small and large intestines: characteristic ulcers surrounded by a haemorrhagic zone.
Nervous system: occasionally cerebral haemorrhages (Sharma and Gautam, 1973).
Bladder: dark-brown urine due to bile pigments.
Skin: exceptionally non-pigmented papules or pustules, necrotic, ulcerative (Manickam et al., 1984).
Eye: exopthalmos observed in cattle in Iran (Baharsefat et al., 1977), exophthalmos and ulceration of the conjunctiva observed in Iraq (Khalifa and Kadhim, 1967), ocular lesions in India (Mallick et al., 1986; Aher et al., 1990).
Specific post-mortem findings have been reported for cases in Bulgaria (Pavlov, 1957; Vulhovski and Pavlov, 1970), Trans-Caucasia (Dschunkowsky and Luhs, 1904), Central Asia (Oboldoueff and Galuzo, 1928), Algeria (Sergent et al., 1945), India (Sen and Srinivasan, 1936; Prasad, 1946; Gautam et al., 1970; Sharma and Gautam, 1971; Gill et al., 1977; Srivastava and Sharma, 1981); Iran (Rafyi and Maghami, 1962; Baharsefat et al., 1977), Iraq (MacHattie, 1935; Khalifa and Kadhim, 1967).
DiagnosisTop of page
For information on diagnosis, see the 'bovine theilerioses' datasheet. The indirect fluorescent antibody test (IFAT) is a prescribed test for international trade, and is described in OIE's Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (OIE, 2013; http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.04.16_THEILIERIOSIS.pdf).
List of Symptoms/SignsTop of page
|Cardiovascular Signs / Jugular pulse||Cattle & Buffaloes:All Stages||Sign|
|Cardiovascular Signs / Tachycardia, rapid pulse, high heart rate||Cattle & Buffaloes:All Stages||Diagnosis|
|Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed||Cattle & Buffaloes:All Stages||Sign|
|Digestive Signs / Bloody stools, faeces, haematochezia||Sign|
|Digestive Signs / Decreased amount of stools, absent faeces, constipation||Cattle & Buffaloes:All Stages||Sign|
|Digestive Signs / Diarrhoea||Cattle & Buffaloes:All Stages||Sign|
|Digestive Signs / Excessive salivation, frothing at the mouth, ptyalism||Sign|
|Digestive Signs / Hepatosplenomegaly, splenomegaly, hepatomegaly||Cattle & Buffaloes:All Stages||Diagnosis|
|Digestive Signs / Mucous, mucoid stools, faeces||Sign|
|Digestive Signs / Pica, depraved appetite||Cattle & Buffaloes:All Stages||Sign|
|Digestive Signs / Rumen hypomotility or atony, decreased rate, motility, strength||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Abnormal proprioceptive positioning, knuckling||Sign|
|General Signs / Ataxia, incoordination, staggering, falling||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Dehydration||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Dysmetria, hypermetria, hypometria||Sign|
|General Signs / Exercise intolerance, tires easily||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Fever, pyrexia, hyperthermia||Cattle & Buffaloes:All Stages||Diagnosis|
|General Signs / Generalized weakness, paresis, paralysis||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Haemorrhage of any body part or clotting failure, bleeding||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Head, face, ears, jaw, nose, nasal, swelling, mass||Sign|
|General Signs / Hypothermia, low temperature||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Icterus, jaundice||Cattle & Buffaloes:All Stages||Diagnosis|
|General Signs / Inability to stand, downer, prostration||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Intraocular mass, swelling interior of eye||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Lack of growth or weight gain, retarded, stunted growth||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Lymphadenopathy, swelling, mass or enlarged lymph nodes||Cattle & Buffaloes:All Stages||Diagnosis|
|General Signs / Neck swelling, mass cervical region||Sign|
|General Signs / Opisthotonus||Sign|
|General Signs / Orbital, periorbital, periocular, conjunctival swelling, eyeball mass||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Pale mucous membranes or skin, anemia||Cattle & Buffaloes:All Stages||Diagnosis|
|General Signs / Petechiae or ecchymoses, bruises, ecchymosis||Cattle & Buffaloes:All Stages||Diagnosis|
|General Signs / Reluctant to move, refusal to move||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Sudden death, found dead||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Swelling skin or subcutaneous, mass, lump, nodule||Sign|
|General Signs / Trembling, shivering, fasciculations, chilling||Cattle & Buffaloes:All Stages||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Cattle & Buffaloes:All Stages||Diagnosis|
|General Signs / Weight loss||Cattle & Buffaloes:All Stages||Sign|
|Nervous Signs / Abnormal behavior, aggression, changing habits||Sign|
|Nervous Signs / Circling||Sign|
|Nervous Signs / Coma, stupor||Cattle & Buffaloes:All Stages||Sign|
|Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless||Cattle & Buffaloes:All Stages||Sign|
|Nervous Signs / Head pressing||Sign|
|Nervous Signs / Hyperesthesia, irritable, hyperactive||Sign|
|Nervous Signs / Seizures or syncope, convulsions, fits, collapse||Sign|
|Nervous Signs / Tremor||Cattle & Buffaloes:All Stages||Sign|
|Ophthalmology Signs / Blindness||Sign|
|Ophthalmology Signs / Corneal edema, opacity||Sign|
|Ophthalmology Signs / Entropion, inverted eyelid||Sign|
|Ophthalmology Signs / Lacrimation, tearing, serous ocular discharge, watery eyes||Cattle & Buffaloes:All Stages||Sign|
|Ophthalmology Signs / Nystagmus||Sign|
|Ophthalmology Signs / Photophobia||Sign|
|Reproductive Signs / Abnormal length estrus cycle, long, short, irregular interestrus period||Cattle & Buffaloes:Heifer,Cattle & Buffaloes:Cow||Sign|
|Reproductive Signs / Abortion or weak newborns, stillbirth||Cattle & Buffaloes:Heifer,Cattle & Buffaloes:Cow||Sign|
|Reproductive Signs / Agalactia, decreased, absent milk production||Cattle & Buffaloes:Cow||Diagnosis|
|Reproductive Signs / Anestrus, absence of reproductive cycle, no visible estrus||Cattle & Buffaloes:Heifer,Cattle & Buffaloes:Cow||Sign|
|Reproductive Signs / Edema of mammary gland, udder||Cattle & Buffaloes:Cow||Sign|
|Reproductive Signs / Warm mammary gland, hot, heat, udder||Cattle & Buffaloes:Cow||Sign|
|Respiratory Signs / Abnormal lung or pleural sounds, rales, crackles, wheezes, friction rubs||Sign|
|Respiratory Signs / Coughing, coughs||Cattle & Buffaloes:All Stages||Sign|
|Respiratory Signs / Dyspnea, difficult, open mouth breathing, grunt, gasping||Sign|
|Respiratory Signs / Epistaxis, nosebleed, nasal haemorrhage, bleeding||Cattle & Buffaloes:All Stages||Sign|
|Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea||Cattle & Buffaloes:All Stages||Diagnosis|
|Respiratory Signs / Mucoid nasal discharge, serous, watery||Sign|
|Skin / Integumentary Signs / Pruritus, itching skin||Sign|
|Skin / Integumentary Signs / Skin edema||Sign|
|Skin / Integumentary Signs / Skin papules||Cattle & Buffaloes:All Stages||Sign|
|Skin / Integumentary Signs / Skin plaque||Cattle & Buffaloes:All Stages||Sign|
|Skin / Integumentary Signs / Skin wheal, welt||Sign|
|Urinary Signs / Haemoglobinuria or myoglobinuria||Sign|
|Urinary Signs / Red or brown urine, pink||Sign|
Disease CourseTop of page
Tropical theileriosis or Mediterranean Coast fever is a non-contagious disease of cattle characterized by fever, enlarged peripheral lymph nodes, emaciation, progressive anaemia and jaundice (Brown, 1990a).T. annulata causes similar disease symptoms across most of its range, as reported in Central Asia (Oboldoueff and Galouzo, 1928; Markov, 1962), in North Africa (Sergent et al., 1945), in the Middle East (Pipano, 1974; El-Metenawy, 2000), in China (Luo and Lu, 1997), in Iran (Rafyi and Maghami, 1962) and in India (Sen and Srinivasa, 1936; Gautam et al., 1970; Sharma and Gautam, 1971; Prasad, 1946). These similarities exist in spite of T. annulata exhibiting extensive strain variation in terms of virulence (Sergent et al., 1945; Pipano, 1974) and molecular diversity (Ben Miled et al., 1994; Katzer et al., 1998; Gubbels et al., 2000). Animals may survive disease but recovery and convalescence can be prolonged and incomplete, leading to permanent debilitation, loss of productivity and a prolonged carrier state (Uilenberg, 1981). Milk production is depressed and may not re-establish itself entirely, even after the following calving (Markov, 1962). In the Asian buffalo, which is probably its original host, T. annulata causes only subclinical or very mild infections (Hadier, 1992; Uilenberg, 1995).
T. annulata causes an acute, mild, sub-acute, per-acute or chronic disease, according to strain virulence and host susceptibility (Sergent et al., 1945; Neitz, 1957; Pipano, 1994; Luo and Lu, 1994). In the acute lethal disease, cattle exhibit increasingly pronounced symptoms from five to seven days after infection, when schizonts become detectable in the lymph node draining the site of infection (Preston et al., 1992).
The early clinical signs include pyrexia coinciding with the appearance of schizonts in the lymph node draining the site of inoculation, and also leucopenia, enlarged superficial lymph nodes, inappetance, drooling, serous nasal discharge, swelling of the eyelids, drooping ears, lowered head, sluggish gait, lacrimation, accelerated pulse, general weakness, decreased milk production and sometimes nervous symptoms. As the disease progresses, the following signs occur: cachexia followed by wasting, marked anaemia with bilirubinaemia and bilirubinurea, superficial lymph nodes become greatly enlarged, thrombocytopenia, conjunctiva icteric with petechial haemorrhages and diarrhoea. During the later stages, the faeces are often mixed with blood and mucus, the skin may bear petechiae and, more rarely, raised nodules containing schizont-infected cells. There may be marked emaciation and recumbency. If erythrocytes do not regenerate, anaemia becomes so severe, and dyspnoea so pronounced, that death ensues 8-15 days after the onset of the disease.
Death may occur within two to three weeks following the proliferation of schizont-infected cells or the haemolytic anaemia resulting from intra-erythrocytic piroplasms. Parasitaemias may reach 60% during the terminal stages of the disease and more rarely, following acute disease, up to 90%. Very rarely, acute infections are accompanied by cerebral symptoms (Sharma and Gautam, 1973; Srivastava and Sharma, 1976). Per-acute disease is fairly common and onset is sudden. Animals with per-acute disease exhibit the symptoms of acute disease, but death preceded by hypothermia occurs within a few days. A panleucopaenia and thrombocytopaenia are common features of acute and per-acute disease syndromes (Prasad, 1946; Laiblin, 1978; Brown, 1990a; Preston et al., 1992). Mild strains may cause subclinical infections, with mild symptoms lasting a few days or sub-acute disease with an irregularly intermittent fever lasting for two to four weeks and less marked symptoms than in acute infections. Animals usually recover but pregnant animals may abort. Chronic disease may persist for a month or more with animals taking more than two months to recover. Sub-acute, acute or chronic forms of the disease sometimes lead to acute episodes and death. Animals dying after a prolonged course show evidence of having suffered a severe aplastic anaemia (Laiblin, 1978; Pipano, 1994). There is evidence for neonatal infections with T.annulata (Mishra et al., 1994).
Anaemia in T. annulata infections has been linked to parasitaemia (Preston et al., 1992) exacerbated by the proliferation of intra-erythrocytic stages (Conrad et al., 1985), autoimmune mechanisms (Hooshmand-Rad, 1976) and erythro-phagocytosis by macrophages (Forsyth et al., 1999). Extensive removal of erythrocytes causes bilirubinaemia and biliruburea in T. annulata infections (Barnett, 1977).
Protective immunity to T. annulata infections
The different parasite stages of T. annulata appear susceptible to attack by a variety of innate and adaptive immune responses (Preston et al., 1999). Parasitized macrophages may be lyzed by CD8+ T-cells and Natural Killer (NK) cells. Macrophage-derived nitric oxide may eliminate sporozoites, trophozoites and schizont-infected cells. Parasite-inhibitory cytokines (e.g. IFN-g ) may kill sporozoites and prevent establishment of trophozoite-infected cells.
EpidemiologyTop of page
The hyalommid vectors of T. annulata occur in sub-humid and semi-arid environments, semi-desert and desert habitats, steppes and dry-grass lands (Galouzo et al., 1958). The most important vectors are Hyalomma anatolicum anatolicum, a three-host tick, and Hyalomma detritum, a two-host tick (Barnett, 1968, 1977; Uilenberg, 1981). These species can act as vectors because all stages have adapted to cattle (Jongejan and Uilenberg, 1994). H. scupense may serve as a field vector (Stepanova, 1976; Markov, 1958; Galouzo et al., 1958), when animals live in close contact (Markov, 1962). Few of the two-host ticks that transmit T. annulata experimentally are likely to be field vectors, because only the adults feed on cattle (Hadani et al., 1963; Jongejan et al., 1983; Um El Hassan et al., 1983). Reports of hereditary transmission(Markov, 1962; Ray, 1950) remain unsubstantiated.
Impact: EconomicTop of page
A global figure for the economic impact and importance of T. annulata is not available, but this parasite is accepted to affect the productivity of perhaps 250 million cattle, causing morbidity in indigenous cattle and mortality of between 40-60% 'improved' cross-bred or exotic animals (Brown, 1990b). It is probably the most important of all tick-borne diseases of domestic stock (Purnell, 1978). The economic impact of T. annulata in India was estimated to be US$ 800m, based on direct losses due to mortality and production losses (milk yield, growth rate, meat, infertility, abortion, calving interval and hides) and the indirect costs of control measures (dipping, vaccination, chemotherapy, veterinary legislation and monitoring) (Brown, 1997). Estimates for Gujarat put the cost of infections at US$ 1.27million for 40,000 cows, with a projected total loss of US$ 210 million per annum for 6.6 million adult cross-bred cows in India (Singh, 1991b). Losses attributable to T. annulata in Tunis were estimated to be approximately US$ 24 per dairy cow, taking into account mortality, treatment costs, milk yield and abortion, and including the effects of subclinical infection as well as overt disease (Darghouth, 1999).
Disease TreatmentTop of page
The napthoquinones parvaquone (Hawa et al., 1988; Gill et al., 1981; McHardy et al., 1983) and buparvaquone (McHardy et al., 1985; McHardy, 1989; McHardy, 1991), and the febrifuginone halofuginone lactate (Schein and Voigt, 1979, 1981), will cure clinical disease resulting from infection with T. annulata or T. parva. However, the therapeutic dose of halofuginone (1.2 mg/kg) often produces side effects (Schein and Voigt, 1979). Parvaquone does not effect a parasitological cure and recovered animals may take several months to return to a normal level of productivity (Dolan, 1986).
Buparvaquone is a safe and effective drug, which can be used both prophylactically (during the prepatent/incubation period) and therapeutically (during patent disease) against T. annulata (McHardy et al., 1985; Dhar et al., 1987, 1988, 1990; McHardy, 1991; Sharma and Mishra, 1990; Singh et al., 1993) (as well as T. parva: McHardy et al., 1985; McHardy, 1991; Dolan et al., 1992). However, in young calves, haematopoiesis-stimulating drugs must be applied together with buparvaquone to avoid the deleterious effects of severe anaemia (Dhar et al., 1988).
Tetracyclines are effective against the schizonts of T. annulata (Gill et al., 1978; Jagdish et al., 1979; Pipano et al., 1981; Mallick et al., 1987) and of T. parva (Dolan, 1981), but only when used in large doses during the prepatent/incubation period of infection (Hashemi-Fershaki and Shad-Del, 1974).
The 8-aminoquinolones - pamaquin and primaquine - are active against the piroplasms of T. annulata (Zhang, 1987, 1997; Luo and Lu, 1997). Extracts of the plant Perganum harmala have a marked suppressive effect on natural infections of T. annulata (Hu et al., 1997).
Prevention and ControlTop of page
Immunization is the chief weapon in the control of tropical theileriosis in highly susceptible dairy breeds of cattle. Attenuated schizont-infected cell culture vaccines remain the main type of vaccine in use (OIE, 2013), notwithstanding progress towards the development of subunit vaccines (Morrison and McKeever, 2006).
The development and application of the attenuated vaccines has been comprehensively described (Pipano, 1989a, b, 1995; Stepanova and Zablostskii, 1989). Immunization may confer protection for periods from a year (Hashemi-Fesharki, 1998) to more than three years (Zablotsky, 1991). The duration of protection in the field depends upon the existence of and level of natural tick-derived sporozoite challenge (Beniwal et al., 2000). Detailed methods for culturing Theileria schizont-infected cells and producing vaccine cell lines have been described by Brown (1983, 1987). The use of vaccination against tick-borne diseases in the development of control strategies in relation to the three main husbandry systems, cattle at pasture, cattle in barns or cattle at zero-grazing, was described by Pipano and Grewal (1990).
Countries where vaccines modelled on the Israeli cell culture vaccine have been developed and used in the field include: Iran (Hashemi-Fesharki and Shad-del, 1973; Hashemi-Fesharki, 1988, 1991, 1998), the former USSR (Stepanova et al., 1976, 1982; Stepanova, 1983; Stepanova et al., 1986; Stepanova and Zablotsky, 1989), India (Singh, 1991a, 1990; Singh et al., 1993a), China (Gansu Provincial Institute of Veterinary Medicine, 1975; Zhang, 1991; Lu and Yin, 1994; Lu and Luo, 1997; Guo et al., 1997; Song, 1997), Turkey (Ozkoc and Pipano, 1981; Ozkoc et al., 1989) and Morocco (Ouhelli et al., 1980). The efficacy of such vaccines in protecting enormous numbers of cattle over very large areas has been demonstrated by the very successful vaccination campaigns in China (Lu and Yin, 1994; Lu and Luo, 1997; Guo et al., 1997; Song, 1997).
In spite of the cross-immunity which exists between stocks of T. annulata throughout its range (Rafyi et al., 1965; Preston and Brown, 1988), the potential for transferring other pathogens has prevented the global use of one vaccine line. Therefore, countries requiring vaccines, for example Tunisia (Darghouth et al., 1996c) or Spain (Viseras et al., 1997; Viseras and Garcia Fernandez, 1999), or in some cases regions within larger countries such as China (Guo et al., 1997; Song, 1997), have had to develop their own individual attenuated vaccines. Aspects that have been studied as part of this include:
Identification of target populations (Darghouth et al., 1997)
The desirability, or otherwise, of the carrier status
The duration of immunity needed
The length of time between boosters (Darghouth, 1999)
The problems of suitability of vaccines for immunizing very young calves and pregnant cattle
- The problem of rejection when the same cell line is used to boost as well as immunize (Beniwal et al., 1997; Grewal et al., 1997; Nichani et al., 1997).
Mechanisms underlying attenuation have been studied with the aim of finding ways of improving/accelerating the attenuation process (Tait and Hall, 1990; Sutherland et al., 1996; Hall et al., 1999; Adamson et al., 2000; Boulter and Hall, 2000).
The infection and treatment method has been investigated with reference to overcoming the problem of vaccinating young calves with a cell-line vaccine (Gill et al., 1976). The drug of choice for this may be buparvaquone (Dhar et al., 1990; McHardy, 1991).
Darghouth (2008) reviews experience with live attenuated vaccines against T. annulata in Tunisia.
Practical problems associated with preparation, storage, transport, administration, possibility of transferring other pathogens and reverting to virulence, are driving work on developing sub-unit vaccines against T. annulata (Tait and Hall, 1990; Preston et al., 1999; Boulter and Hall, 2000; Hall et al., 2000). These include investigations on genetic diversity (Katzer et al., 1998; Gubbels et al., 2000; Morrison and McKeever, 2006).
Some further information on prevention and control, including vector control, breeding of resistant cattle and combinations of different control methods, is provided in the 'bovine theilerioses' datasheet.
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