A review on Babesia spp. and tick vectors in animals in Iran

Document Type : Review article

Author

Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.

Abstract

Babesiosis is an important tick-borne disease that affects a wide range of domestic and wild animals and occasionally humans in tropical and subtropical countries. So far, More than 100 different Babesia species have been identified in animals. Iran is one of the largest countries in the Middle East. The existence of two chains of mountains namely Zagros and Alborz has provided a number of climatic variations with different flora and fauna. These different climatic zones in Iran are potentially favorable for a large variety of tick vectors transmitting blood pathogen protozoa like Babesia spp. and Theileria spp. in animals. In the last decade, many molecular studies have been performed to identify Babesia spp. and tick vectors in different parts of Iran.  This review article aims to provide useful information about the history, characters, geographical distribution, and prevalence of Babesia species and their related tick vectors in animals in Iran. 

Keywords

Main Subjects

Introduction

Babesiosis is an important tick-borne disease in domestic and wild animals. The causative agent and vectors for this disease are Babesia spp. and Ixodid ticks, respectively [ 1 ]. Babesia species live and multiply as ‘piroplasms’ in erythrocytes of the vertebrate host, and in contrast to erythrocytic stages of Plasmodium do not contain pigment [ 2 ]. The female tick usually is infected by ingesting protozoa in the blood meal and transmitting them to new hosts as sporozoites in the tick's saliva of the next generation, larvae, nymphs, and adults. The main clinical signs of babesiosis are fever, hemoglobinuria, anemia, and icterus [ 2 ]. Babesiosis has a wide geographical distribution in temperate, tropical, and subtropical regions. Iran is located in the western Palearctic countries with a high diversity of hard ticks [ 3 ] that could act as a vector for Babesia spp. in animals [ 3 ]. Advances in molecular biology methods have led to changes in the identification of Babesia species and their vectors in the world. Many molecular studies have been conducted on Babesia spp. identification in domestic animals in Iran from 1998 to 2015. Based on these results, two systematic reviews were also published about babesiosis in sheep, goats, cattle, and horses [ 4 , 5 ]. This review provides useful information about the history, characters, geographical distribution, and prevalence of Babesia species, and their related tick vectors in animals in Iran.

History of Babesia

Babesia, also called Nuttallia, is an apicomplexan parasite that infects red blood cells and is transmitted by hard ticks. It was discovered in the red blood cells of cattle by the Romanian bacteriologist Victor Babes in 1888. He later observed a similar organism in sheep blood [ 6 ]. Five years later, Smith and Kilbourne showed the presence of an intraerythrocytic parasite in dairy cattle with Texas cattle fever, a disease that had long stricken cattle ranchers in the southern USA [ 7 ]. They were given the name Pyrosoma bygeminum, and showed that ticks play a major role in the transmission of this disease. This was the first description of an arthropod-transmitted, pathogen of vertebrates. Starcovici chose the name Babesia for these organisms in 1893 [ 8 ]. Lignieres described two forms of Babesia as B. bigemina and B. bovis in cattle in Argentina in 1903 [ 9 ]. In Iran, Delpy identified B. ovis in sheep for the first time in 1936 [ 10 ]. The first human babesiosis was reported in a splenectomized Yugoslavian farmer in 1957. After the initial case in Europe, a case caused by B. microti was diagnosed in a splenectomized patient from California, USA, in 1966. Babesia crassa as a large Babesia species was isolated for the first time in the world from an Iranian sheep in 1981 [ 13 ].

Taxonomy, transmission, and morphology

The genus Babesia belongs to the phylum Apicomplexa, and the family Babesiidae. Babesia is a relatively piriform, round, or oval parasite; the apical complex contains a polar ring, rhoptries, and subpellicular tubules. Micronemes and conoids are present in some stages and in some species [ 14 ]. Based on the merozoite size and comparison with erythrocyte radius, Babesia spp. are divided into large and small groups. The lengths of small and large Babesia are 1.0 to 2.5 μm and 2.5 to 5.0 μm, respectively. The morphometric method has no clear genetic basis, because the size and morphology of Babesia spp. may be changed during the asexual stage within red blood cells or when infects a non-specific host [ 15 , 16 ]. So far, over 100 Babesia species have been identified in vertebrate hosts. Of those, eighteen species have been found to cause babesiosis in domestic mammals, including pigs, horses, cattle, sheep, goats, cats, and dogs. Most Babesia species have been reported in rodents, cattle, and carnivores (Table 1).

Host Species Morphology Tick vector Distribution
Cattle B.bovis Small Boophilus,Rhipicephalus Africa, America, Asia, Australia, Europe
B.Bigemina Large Boophilus,Rhipicephalus Africa, America, Asia, Australia, Europe
B.major Large Haemaphysalis Asia, Europe
B. occultans Large Hyalomma Africa
B. ovata Large Haemaphysalis Asia
B. divergens Large Ixodes, Europe
B. sp. Kashi Large Hyalomma China
Buffalo B. orientalis Small Rhipicephalus Asia
B. bovis Small Boophilus,Rhipicephalus Asia, America
B. bigemina Large Boophilus,Rhipicephalus Asia, America
Horse, Donkey B.equi Small Asia, Europe, America
B.caballi Large Dermacentor, Hyalomma, Rhipicephalus Asia, Europe, America
Pig B.trautammani Rhipicephalus Africa, Europe
Sheep, Goat B.ovis Small Rhipicephalus Africa, Asia, Europe
B.motasi Large Haemaphysalis Africa, Asia, Europe
B.crassa Small Unknown Asia
Dog B.vogeli Large Rhipicephalus sanguineus Africa, America, Asia, Australia, Europe
B.conradae Small America
B.gibsoni Small Haemaphysalis longicornis, Rhipicephalus Africa, America, Asia, Australia, Europe
B.rossi Large Haemaphysalis South Africa
B.canis Large Dermacentor Europe
Cat B.felis Small Unknow South Africa
B. cati Unknow India
Table 1.Different Babesia species and tick vectors with geographical distribution in domestic animals [ 1 ].

Life cycle

The life cycle of Babesia spp. consists of at least the asexual and sexual stages of reproduction that occur within the vertebrate host and tick vector, respectively. The sporozoites of the tick’s salivary glands are generally transmitted to the vertebrate host 2-3 days after tick attachment. The sporozoites change to merozoites and enter red blood cells and divide by binary fission into new merozoites. Infected erythrocytes eventually rupture and release organisms that invade and multiply within other red blood cells. Some of the merozoites become pre-gametocytes that cannot be distinguished by a light microscope. When the tick vectors ingest the infected blood of the vertebrate host, the merozoites are microscopically detectable in the tick's gut after 10 hours [ 16 ]. The pre-gametocytes develop into gametocytes and begin to form ray bodies at the anterior of the piroplasm. The ray bodies form gametes and fuse to produce a motile zygote termed ookinete, which enters the gut epithelium cells. The ookinete starts meiotic division, resulting in many kinetes productions. At this stage, the kinetes migrate via hemolymph to different tick tissues such as ovarian cells. The infection of eggs leads to transovarial transmission. Some kinetes enter the salivary gland cells where a large multinuclear sporont is finally formed, giving rise to thousands of small sporozoites, which are injected during the feeding act and lead to transstadial transmission (Figure 1) [ 17 , 18 ].

Babesia spp. infection in domestic animals in Iran.

Figure 1. The life cycle of Babesia ovis [ 1 ].

Cattle

In Iran, the main species of Babesia in cattle are B. bigemina and B. bovis [ 19 ]. The first outbreak of babesiosis due to B. bovis was reported from a dairy farm in the Rasht area [ 20 ]. B. bovis localizes near the margin of the erythrocyte and is clearly smaller than B. bigemina and larger than Theileria annulata. The shape of B. bovis is ring form or ovoid. The erythrocytic stage of B. bigemina is large, round, oval, or pear-shaped and fills the whole erythrocyte when divided [ 17 ]. Few studies have been performed on bovine babesiosis compared to ovine babesiosis in Iran. It seems that B. bovis and B. bigemina are more common in cattle in western and northwestern Iran (Table 2). Among Ixodid ticks, B. annulatus, R. Bursa, and R. sanguineous could be the vector for Babesia spp. in dairy cattle [ 23 , 24 ]. The large B. occultance was recently reported from two cattle in the Miandoab area by molecular methods [ 27 ].

Year Babesia species Tick vector Province or Area Prevalence Diagnostic methods References
1977 B. bovis B. annulatus Rasht - Microscopic examination [ 20 ]
2012 B.bigemina - Tabriz - Microscopic examination, PCR [ 21 ]
2012 B.bigemina Kurdestan 2.1% Microscopic examination [ 22 ]
2012 Babesia spp. R.sanguineus and R. bursa Kurdestan and West Azarbijan PCR [ 23 ]
2017 B.bigemina , B.bovis B.annulatus, R.sanguienus, R.bursa Urmia 4.2% Microscopic examination , PCR [ 24 ]
2020 B.bigemina, B.bovis - East and West Azarbijan 25.49% Microscopic examination , PCR [ 25 ]
2020 B.bigemina, B.bovis - Mazandaran 33.33% PCR [ 26 ]
2021 B.occultans - Miandoab - Microscopic examination, PCR [ 27 ]
Table 2.Reported Babesia species and related tick vectors in cattle in Iran

Sheep and goats

Three Babesia species including B. ovis, B. motasi, and B. crassa have been reported in infected sheep and goats in Iran (Table 3). Babesia ovis is a small round piroplasm, situated usually at the periphery of the red blood cells of infected sheep [ 17 ]. This species is widespread in almost all parts of Iran [ 28 , 29 ]. Babesia motasi, as a large species is less prevalent in Iran [ 30 ]. Babesia ovis is high pathogenic and causes anemia and hemoglobinuria, while B. motasi appears moderately virulent [ 31 ]. Babesia crassa is a large species that was isolated from an Iranian sheep. It is characterized by an oval tetrad form in infected erythrocytes. The protozoon appears to be nonpathogenic to intact sheep and goats [ 13 ]. The outbreaks of ovine babesiosis are recorded in sheep and goats at the age of 6- 12 months each year [ 32 - 33 ]. Potential vectors for B. ovis could be R. bursa, R. sanguineous, and R. turanicus [ 35 , 36 ]

Year Babesia species Tick vector Province or Area Prevalence Diagnostic methods Referncesc
1936 B. ovis - - - Microscopic examination [ 10 ]
1966 B.motasi - West of Iran - Microscopic examination [ 32 ]
1981 B.crassa - - - Microscopic examination [ 13 ]
1998 B.ovis - Caspian sea, Mountainous, Persian gulf and desert climates 15.93%, 58.81%, 12.04%, 13.22% Serology [ 34 ]
2002 B.ovis , B.motasi R.sangueineus, Hy.marginatum Mashhad 24.6% , 0.5% Microscopic examination [ 35 ]
2003 B.ovis , B.motasi - Mashhad 14%,0.5% Microscopic examination [ 36 ]
2006 B. ovis - Khouzestan 47.5% Serology [ 37 ]
2006 B. ovis, B.motasi - - Microscopic examination, PCR [ 38 ]
2007 B.ovis R.bursa, R.sangueinus, R.turanicus PCR [ 39 ]
2008 B.ovis - PCR [ 40 ]
2010 B.ovis - Different areas of Iran 24.67% Microscopic examination, PCR [ 41 ]
2012 B.ovis - - - Reverse line blot [ 42 ]
2013 B.ovis - Tabriz 14% PCR [ 43 ]
2013 B.ovis Dargaz, Kalat 0.99% Microscopic examination, PCR [ 44 ]
2013 B.ovis, B.motasi - Mazandarn province 5% Microscopic examination, PCR [ 45 ]
2014 B.ovis R.turanicus, Hya.marginatum North khorsan province Microscopic examination, PCR [ 46 ]
2014 B.ovis R.bursa West Azarbijana 16.7% Microscopic examination, PCR [ 47 ]
2017 B.ovis D. Niveus, D.marginatus Ardabil PCR [ 48 ]
2017 B.ovis - Lorestan PCR [ 48 ]
2017 B.ovis R.sanguienus, Hy,suspense Gonbad Kavoos, Marvaeh tapaeh - PCR [ 50 ]
2018 B.ovis East azerbijan 11.4% PCR [ 51 ]
2020 B.ovis Baneh 86% PCR [ 52 ]
2020 B.ovis, B.motasi - Tonkabon, Ramsar 6%,1% PCR [ 53 ]
Table 3.Reported Babesia species and related tick vectors in sheep and goats in Iran

Horse and donkey

Babesia equi and B. cablli were reported from horses in different areas of Iran (Table 4). Studies have shown that B. equi is more prevalent than B. caballi in Iranian horses and donkeys. The presence of B. caballi and T. equi was confirmed in 1940 by microscopic and molecular examination [ 54 ]. A few case reports of babesiosis due to B. caballi and B. equi have been published on horses in different parts of Iran from 1994 to 2000 [ 55 - 58 ]. In a study, B. equi infection was determined in donkeys of North Khorasan province by microscopic and molecular methods [ 67 ]. The name of B. equi has recently been changed to Theileria equi, because the sporozoites of T. equi first evade the lymphocytes and multiply by schizogony. After rupture of infected lymphocytes, the released merozytes enter the red blood cells and change to rounded, amoeboid, and a Maltese cross-shaped phenotype [ 2 ]. The vectors of T. equi could be Hyalomma spp. and also Rhipicephalus spp.. The eggs of these ticks were not infected with ookinetes to indicate transovarial transmission [ 17 ]. The merozoites of B. caballi are large and pear-shaped. They are produced by binary fission. Babesia infections are always detected in the eggs of tick vectors that could be transmitted to larvae in the next generation [ 17 ].

Year Babesia species Tick vector Province or Area Prevalence Diagnostic methods Referncesc
2000 B.cabali - Fars province - Microscopic examination [ 57 ]
2000 B. cabali, B. equi - Mashhad - Microscopic examination [ 58 ]
2013 B.cabali, B.equi North Khorasan Province 2%, 48% Seology [ 59 ]
2014 B.equi Hya.excavatum, Rh.bursa North Khorasan Province 45% Microscopic examination, serology , PCR [ 60 ]
2014 B.cabali North Khorasan Province 4.8% Microscopic examination, Serology [ 61 ]
2014 B.cabali, B.equi Urmia area 2.08%, 6.26% Microscopic examination, PCR [ 62 ]
2014 B.equi - Khuzestan Province 28.5% PCR [ 63 ]
2014 B.equi Yazd area 4.7%, 22.8% Microscopic examination, PCR [ 64 ]
2014 B.equi - Mianeh area 4.1% Microscopic examination [ 65 ]
2015 B.equi - Ahvaz area Microscopic examination,PCR [ 66 ]
2015 B.equi - North Khorasan Province 3.77% , 50.94% Microscopic examination,PCR [ 67 ]
2016 B.equi Piranshar area 9.6%, 96% Microscopic examination , PCR [ 68 ]
2017 B.equi, B.caballi - Isfhan, Sharekord - PCR [ 69 ]
2017 B.equi - Kurdistan 1.61% Microscopic examination , PCR [ 70 ]
2018 B.equi - West Azarbijan 3.2%, 27.7% Microscopic examination , PCR [ 71 ]
Table 4.Reported Babesia spp and related tick vectors in horses and donkeys in Iran

Dog

For the first time, Babesia canis, and B. gibsoni were reported in the blood smear of splenectomized dogs and foxes from the north of Iran in 1973 [ 72 ]. Further study was shown that the isolated strain is mild and does not produce clinical signs in experimentally infected dogs. Many studies have reported the large Babesia spp. in dogs of different parts of Iran (Table 5). Babesia canis as a large Babesia has three subspecies, B. canis vogeli, B. canis rossi, and B. canis canis. They are different in genotype, geographic distribution, pathogenicity, and vector-specificity [ 73 ]. Babesia gibsoni, B. conradea, and Theileria annae are termed small canine Babesia. Among different hard tick species, it has been reported that R. sanguineous could act as a vector for B. vogeli and B. canis, and Haemaphysalis spp. as a veorct for B. rossi and B. gibsoni [ 73 ].

Year Babesia species Tick vector Province or Area Prevalence Diagnostic methods Referncesc
1973 Babesia canis Babesia gibsoni - Mazandaran Province 0.64% Microscopic examination [ 72 ]
2012 B.canis Shiraz - PCR [ 74 ]
2013 B. canis Khousestan Province 3.75% Microscopic examination [ 75 ]
2014 B.canis Charmahal Bakhtiri 7.5% PCR [ 76 ]
2016 B.gibsoni Kerman province 5% PCR [ 77 ]
2020 B.canis vogeli Shariar - PCR [ 78 ]
2021 B.canis vogeli Hamadan 4% PCR [ 79 ]
2022 B.canis canis Tehran - PCR [ 80 ]
Table 5.Reported Babesia species in dogs in Iran

Camel

So far, a specific Babesia species has not been reported in camels worldwide. Based on molecular methods, Babesia species related to cattle and horses have been found in camels [ 81 ]. Babesia caballi and T. equi have been detected in camels in Iran [ 82 - 84 ].

Rodents

Babesia microti, a species of rodent origin, has been recognized as an agent of human babesiosis in the world [ 1 ]. There are a few reports about the presence of Babesia microti in Iran [ 85 - 87 ].

Conclusion

This review presented a comprehensive summary of research findings on the identification, prevalence, and distribution of Babesia species and their related vectors in domestic animals in Iran. In the last decade, many molecular studies have been performed to identify Babesia spp. and tick vectors in different parts of Iran. However, there is no information about Babesia infection in cats and wild animals. Further molecular and experimental methods will be needed to better understand the epidemiology of Babesia species and their related tick vectors in domestic and wild animals.

Competing Interests

The authors declare that they have no conflict of interest.

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  • Receive Date: 02 April 2022
  • Accept Date: 10 June 2022

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