Babesia,[3][4] also called Nuttallia,[5] is an apicomplexan parasite that infects red blood cells and is transmitted by ticks. Originally discovered by Romanian bacteriologistVictor Babeș in 1888; over 100 species of Babesia have since been identified.[6][7]
Babesia comprises more than 100 species of tick-borne parasites that infect erythrocytes (red blood cells) in many vertebrate hosts.[8]
Babesia species infect livestock worldwide, wild and domestic vertebrate animals, and occasionally humans, where they cause the disease babesiosis.[9][7] In the United States, B. microti is the most common strain of the few that have been documented to cause disease in humans.
Babesia is a protozoan parasite found to infect vertebrate animals, mostly livestock mammals and birds, but also occasionally humans. Common names of the disease that B. microti causes are Texas cattle fever, redwater fever, tick fever, and Nantucket fever.[7] The disease it causes in humans, babesiosis, is also called piroplasmosis.[9]
Babesia microti, however, is not part of the genus Babesia. Due to historical misclassifications, the protozoan has been labeled with many names, including Nuttallia,[5] and was renamed from Babesia microti to Theileria microti based on evidence from 2006. Its genetic sequence, published in 2012, shows that the species belongs to neither Babesia nor Theileria, but instead to a separate genus.[10] Another "western" group is also separate from core Babesia.[2]
The avian Babesia species are characterized as having ring and amoeboid forms, and fan-shaped or cruciform (cross-shaped) tetrad schizonts. Developing parasites have only been reported in red blood cells.[11]
History
For centuries, the animal disease was known to be a serious illness for wild and domesticated animals, especially cattle. In 1888, Victor Babeș first identified the causative agent in Romania and believed it to be due to the bacterium he named Haematococcus bovis. He documented the disease by describing signs of a severe hemolytic illness seen uniquely in cattle and sheep.[7][12]
In 1893, Americans Theobald Smith and Fred Kilborne identified the parasite as the cause of Texas cattle fever, the same disease described by Babeș. They also identified the tick as the transmitting agent, a discovery which first introduced the concept of arthropods functioning as disease vectors.[13]
It was believed to be a disease that only affected nonhuman mammals, but in 1957, the first case of babesiosis was seen in a human.[9] The person had been splenectomized, as were all people diagnosed with babesiosis until 1969, when the first case of babesiosis was diagnosed in a person who still had their spleen. This proved the parasite was a potential pathogen in anyone.[14]
Genetics
Babesia species show host specificity, allowing many different subspecies of Babesia to emerge, each infecting a different kind of vertebrate organism.[15] While B. bovis and Babesia bigemina prefer to infect cattle in tropical environments, they can infect other animals, such as the white-tailed deer.[15] Therefore, while the organism has the capacity to display host specificity, and thus increase transmission effectiveness, it can still infect a variety of hosts.[15] It achieves this through mutations and natural selection. In different environments, individual protozoa may develop mutations, which when they increase the protozoa's fitness, allow the population to increase in number. This specificity explains why Babesia species have such great genetic diversity.[15]
Babesia selfishly persists long-term in the host's system: The host gains no benefit from the parasite invasion and only suffers. This allows the parasite to exploit all resources offered by the host, to increase in number, and to increase the rate of transmission.[15] Too lethal an infection results in the host's death and the parasite is unable to spread, which is a loss from an evolutionary standpoint.[15] Different species of Babesia are able to withstand the stress of the host's immune system. Infection typically stimulates the innate immune system, and not the humoral immune system.[15] This results in control of the infection, but also persistence and not clearance of the parasite.[15]
Genomics
The genome of B. microti has been sequenced and shows that the species does not belong to either Babesia or Theileria, but instead to a separate genus.[10]As of 2013[update], it is known that the mitochondrial genome is linear like other sequenced Apicomplexa mitochondrial genomes, although it was initially reported that it was circular.[16]
The lifecycle of B. microti, which is typical of parasites in the genus, requires a biological stage in a rodent or deer host. It is transmitted by ticks of the family Ixodidae between these hosts. To begin, the tick as the definitive host becomes infected itself, as it takes up gametocytes when attached for a blood meal. It also introduces the Babesia into the intermediate host (e.g. cattle) when taking a blood meal. As Babesia enter the animal's red blood cells (erythrocytes), they are called sporozoites. Within the red blood cell, the protozoa become cyclical and develop into a trophozoite ring. The trophozoites moult into merozoites, which have a tetrad structure coined a Maltese-cross form.[17] Trophozoite and merozoite growth ruptures the host erythrocyte, leading to the release of vermicules, the infectious parasitic bodies, which rapidly spread the protozoa throughout the blood.[9] Rather than producing more and more trophozoites, some of the merozoites produce gametocytes. The gametes are fertilized in the tick gut and develop into sporozoites in the salivary glands. These are the sporozoites the infected tick introduces when it bites an intermediate host. Even as an incidental host, the phase changes that occur in the parasite are the same within humans as in the biological hosts. Babesia can be diagnosed at the trophozoite stage, and can also be transmitted from human to human through the tick vector, through blood transfusions, or through congenital transmission (an infected mother to her baby).[18][6]
Lifecycle of Babesia
Seasonality
Temperature
Cold weather completely interrupts transmission.[19] The emergence of tick-borne diseases has been found to coincide with climate change.[20] The correlation between climate change and the incidence of tick-borne diseases is not known to be strong enough to count as a major factor.[20]
Humidity
High humidity and rainfall accommodate ticks carrying Babesia.[21] This may explain why B. bigemina infection in cattle in the hilly region of Meghalaya has increased.[21] The lifespan and number of generations of B. microplus correlate with increasing the longevity of larvae and the number of annual generations.[21] Warm, dry weather interferes with the Babesia lifecycle within the tick.[19] Warm, wet weather increases the intensity of infestation—the population is able to thrive due to the relatively fluid environment, making water and nutrients more accessible.[19]
Transmission
Babesia species are spread through the saliva of a tick when it bites. Already at its nymphal stage, a tick bites into the skin for a blood meal. The tick, if not removed, stays attached for three to four days, with longer periods of feeding associated with a higher probability of acquiring the parasite. The parasite can survive in the tick as it molts through its various developmental stages, resulting in all tick stages being potentially infectious. Some species of Babesia can be transmitted from a female tick to its offspring before migrating to salivary glands for feeding.[9]B. microti, the most common species in humans, has not been shown to transmit transovarially.[6]
Ticks of domestic animals that transmit Babesia and cause much disease include the very widespread cattle ticks, Rhipicephalus (Boophilus) microplus, and R.(B.) decoloratus. These ticks have a strict one-host feeding cycle on cattle, so the Babesia can only be transmitted by the transovarial route.
In the Americas, Ixodes scapularis is the most common vector. This hard tick, commonly known as a deer tick, is also the vector for other tick-associated illnesses, such as Lyme disease. Many species of Babesia only infect nonhuman mammalian hosts, most commonly cattle, horses, and sheep. B. microti and B. divergens are the two main pathogenic species in humans. Their reservoirs are theorized to be the white-footed mouse (Peromyscus leucopus), voles from the Microtus genus, and the white-tailed deer (Odocoileus virginianus).[22] These woodland species are hypothesized reservoirs because although they are known to harbor the disease, complete reservoir competence has not yet been shown.[23]
Most cases of transmission between humans are attributed to a tick vector. As of 2003, the Centers for Disease Control and Prevention (CDC) acknowledged more than 40 cases of babesiosis contracted from transfusions of packed red blood cells (PRBC), as well as two infections documented from organ transplantation. PRBC transfusions that cause infections were identified through testing the blood donor for B. microti antibodies.[24] The occurrence of Babesia transmission through PRBC blood transfusions puts pressure on governmental organizations (such as the CDC) to heighten standard measures for screening blood donations.[citation needed]
Transmission is also possible through congenital transmission (from an infected mother to her baby). As symptoms may not appear, many women may not be aware they are infected during pregnancy, so a measurement of congenital transmission rate is not known at this time.[18]
Currently, no vectors for avian Babesia have been identified, but they are assumed to be ticks.[11]Babesia species require competent vertebrate and invertebrate hosts to maintain transmission cycles.[25]
Epidemiology
Of the species to infect humans, B. microti is most common in the Americas, whereas B. divergens is the predominant strain found in Europe. Endemic areas are regions of tick habitat, including the forest regions of the Northeastern United States and temperate regions of Europe.[26] Ixodidae, the tick vectors of B. microti, also transmit the better-known Borrelia burgdorferi, the causative agent of Lyme disease. For reasons that remain unclear, in areas endemic to both Lyme disease and babesiosis, Lyme disease transmission prevails and is more predominant in the region.[9] Prevalence of babesiosis in malaria-endemic regions remains unknown due to the likelihood of misdiagnosis as malaria.[27] As the disease results in a high number of asymptomatic individuals, many populations can possess high seroprevalence without much documentation of illness. For example, in Rhode Island and Nantucket, seroprevalence has been measured to be 20–25%.[9] Prevalence of babesiosis is mostly documented from May to September, when tick activity in endemic regions is high.[26]
The avian Babesia include 15 species, and four Babesia species have been reported from sea hosts. B. poelea was described from brown boobies (Sula leucogaster) on Sand Island, Johnston Atoll, Central Pacific.[28]B. poelea was reported from a masked booby (Sula dactylatra melanops) from Desnoeufs Island, Amirantes, Seychelles.[29]B. peircei has been observed in two species of penguins, the jackass penguin (Sphenicus demersus) from South Africa and the little penguin (Eduyptula minor) from southern Australia.[30][31]B. bennetti was associated from the yellow-legged gull (Larus cachinnans) from Benidorm Island off the coast of Spain.[31]B. uriae was found in common murres in California.
About 40 cases of human babesiosis, caused by intraerythrocytic protozoans (protozoa inside red blood cells) of the genus Babesia, were reported in Europe.[32]
Disease
Bovine babesiosis caused by B. bovis is an important constraint for cattle industries worldwide.[citation needed]
Signs of infection with B. microti usually arise one to eight weeks after a bite from an infectious tick.[26] Infections from B. divergens have a shorter latent period, usually ranging from one to three weeks.[27] The severity of B. microti infections varies. For 25% of cases in adults and 50% of cases in children, the disease is asymptomatic or mild with flu-like symptoms. In other cases, symptoms are characterized by irregular fevers, chills, headaches, general lethargy, pain, and malaise.[9] In severe cases, effects of parasitic multiplication, symptoms such as hemolytic anemia, jaundice, shortness of breath, and hemoglobinuria have been documented.[7][27] Individuals with normal immune function and healthy spleens often recover without treatment.[9]
Splenectomized patients are more susceptible to contracting the disease and can die within five to eight days of symptom onset.[26] They have severe hemolytic anemia, and occasional hepatomegaly has been documented. Parasitemia levels can reach up to 85% in patients without spleens, compared to 1–10% in individuals with spleens and effective immune systems.[27]
Complications include acute respiratory failure, congestive heart failure, and kidney failure. Infections can be fatal in 5–10% of hospitalized patients, with increased risk of death in the immunosuppressed, the elderly, and those also infected with Lyme disease.[27]B. divergens infections have a much higher fatality rate (42%) and present with more severe symptoms. Infected individuals experience hemoglobinuria followed by jaundice, a persistently high fever, chills, and sweats. If left untreated, B. divergens infections can develop into shock-like symptoms with pulmonary edema and kidney failure.[27]
In birds
The pathogenicity of B. uriae for murres is currently unknown. Birds were found with lesions, anemia and respiratory difficulty, and tissues of avian hosts were affected.[11]B. peircei infections can cause mild anemia, leukocytosis, and impairment of hepatic function in African penguins.[33]
Diagnostic tests
As a protozoan parasite, the most effective way to identify Babesia infection is through blood sample testing.
Morphology
Babesia species enter red blood cells (erythrocytes) at the sporozoite stage. Within the red blood cell, the protozoa become cyclical and develop into a trophozoite ring. The trophozoites moult into merozoites, which have a tetrad structure coined a Maltese-cross form.[17] This tetrad morphology seen with Giemsa staining of a thin blood smear is unique to Babesia, and distinguishes it from Plasmodium falciparum, a protozoan of similar morphology that causes malaria. Trophozoite and merozoite growth ruptures the host erythrocyte, leading to the release of vermicules, the infectious parasitic bodies, which rapidly spread the protozoa throughout the blood.[9] It is important to pay attention to particular morphologies of Babesia in blood smears, because of its great similarity to the malarial parasite Plasmodium falciparum. This has resulted in many patients with babesiosis being misdiagnosed. The few distinguishing factors for Babesia include protozoa with varying shapes and sizes, the potential to contain vacuoles, and the lack of pigment production. Trophozoites appearing in a tetrad formation within an erythrocyte are also indicative of Babesia.[citation needed]
Despite much study of babesiosis and malaria, misdiagnosis with blood smear can be frequent and problematic. To supplement a blood smear, diagnoses should be made with an indirect fluorescent antibody (IFA) test, which has a much higher specificity than stained blood smears, with antibody detection in 88-96% of infected patients.[6] Diagnostic measures through antibody testing are also particularly useful for identifying serum prevalence in asymptomatic individuals. Due to the transmissibility of Babesia through blood transfusions, IFA testing would be an effective means of screening for the disease in blood donations.
Historically, babesiosis diagnosis was carried out with xenodiagnosis in hamsters for B. microti and in gerbils for B. divergens.[9] This diagnostic technique has been abandoned in favor of faster diagnostic measures.
Treatment
Several methods are available to manage and treat babesiosis in animals.[citation needed]
In humans, many spontaneously recover, having only experienced mild symptoms not diagnosed as the disease. This is almost always seen in B. microti infections, which are generally more common in the United States. For B. divergens and more severe B. microti infections, the standard treatment historically for symptomatic individuals was oral or intravenous clindamycin with oral quinine.[6] With the results of research completed in 2000, however, treatment regimens have been increasingly leaning towards oral atovaquone with oral azithromycin. The latter are preferred, as they are equally effective in all but the most severe cases and exhibit fewer associated adverse reactions.[34] In severe cases, blood exchange transfusions have been performed to lower the parasitic load in an individual.[9] Other measures include addressing and correcting abnormal clinical signs.[7]
In seabirds, primaquine has been used in a study to show effective treatment on infected hosts.[35] Treatment for babesiosis consisted of primaquine (1mg/kg PO q24h for 10 days; primaquine phosphate 1.76%m/v in stabilized solution, Primaquin Solution, MedPet Ltd, Benrose, South Africa). After, treatment was followed by a phospholipid supplement (1 capsule/bird PO q24h for 12 days; deoiled, enriched phospholipids from soybeans, 300mg/capsule, Essentiale Extreme, Sanofi Aventis Ltd, Midrand, South Africa); as an attempt to mitigate potential hepatotoxic effects of primaquine. To prevent transmission of Babesia and other tickborne pathogens, all birds with visible ectoparasites are treated with pesticide powder (carbaryl 50 g/kg) upon admission, and the facilities are thoroughly cleaned on a daily basis.[35]
Prevention in animals
In 1906, efforts were made to eradicate the tick vector of bovine babesiosis in the United States. This eradication was recorded as being successfully completed.[7] The disease was eradicated from the United States by 1943, except for a permanent quarantine area along the Texas/Mexico border, where cattle fever ticks are still found.[36]
Effective control can be achieved by vaccination with live attenuatedphenotypes of the parasite. The vaccines have a number of drawbacks, so better, safer vaccines are still being researched.[citation needed] In recent[when?] years, a number of parasite proteins with immunogenic potential have been discovered. Through polymerase chain reaction, genetic sequencing, and bioinformatics analysis of the genes, a high degree of conservation (98–100%) was found among Brazilian isolates of B. bovis and the T2Bo isolate. Thus, these genes are considered for inclusion in a recombinant cocktail vaccine for cattle babesiosis caused by B. bovis.[citation needed]
Prevention in humans
The most effective public health measure for Babesia is to avoid tick exposure. This can be through personal prevention such as avoiding tick-infested areas (especially during high tick season between May and September), remaining covered with light clothing, searching for ticks after being outdoors, and removing discovered ticks from the skin.[27] Other measures include applying DEET, a common repellent that is effective against ticks and insects. (For people who react adversely to DEET, alternative insect repellents should be used.) On a state level, if health departments are particularly motivated, tick elimination is a possibility. In 1906, efforts were made to eradicate the tick vector of the bovine disease form of babesiosis in the United States. This eradication was recorded as being successfully completed four decades later.[7]
Complete eradication through vector control would be a long-term project, which would significantly reduce the prevalence of both babesiosis and Lyme disease, but as public health departments are often short on funding, preventive measures are more recommended.[citation needed]
Due to the relatively low prevalence of the human disease and the presence of several reservoirs, babesiosis has not been a candidate for vaccines. In regions where ticks of domestic animals are routinely controlled with chemical acaricides to reduce incidence of infection with B. bovis and B. bigemina, the risk to humans from these parasites is reduced.
Related Research Articles
Babesiosis or piroplasmosis is a malaria-like parasitic disease caused by infection with a eukaryotic parasite in the order Piroplasmida, typically a Babesia or Theileria, in the phylum Apicomplexa. Human babesiosis transmission via tick bite is most common in the Northeastern and Midwestern United States and parts of Europe, and sporadic throughout the rest of the world. It occurs in warm weather. People can get infected with Babesia parasites by the bite of an infected tick, by getting a blood transfusion from an infected donor of blood products, or by congenital transmission . Ticks transmit the human strain of babesiosis, so it often presents with other tick-borne illnesses such as Lyme disease. After trypanosomes, Babesia is thought to be the second-most common blood parasite of mammals. They can have major adverse effects on the health of domestic animals in areas without severe winters. In cattle, the disease is known as Texas cattle fever or redwater.
Plasmodium falciparum is a unicellular protozoan parasite of humans, and the deadliest species of Plasmodium that causes malaria in humans. The parasite is transmitted through the bite of a female Anopheles mosquito and causes the disease's most dangerous form, falciparum malaria. P. falciparum is therefore regarded as the deadliest parasite in humans. It is also associated with the development of blood cancer and is classified as a Group 2A (probable) carcinogen.
Hepatozoon is a genus of Apicomplexa alveolates which incorporates over 300 species of obligate intraerythrocytic parasites. Species have been described from all groups of tetrapod vertebrates, as well as a wide range of haematophagous arthropods, which serve as both the vectors and definitive hosts of the parasite. By far the most biodiverse and prevalent of all haemogregarines, the genus is distinguished by its unique reciprocal trophic lifecycle which lacks the salivary transmission between hosts commonly associated with other apicomplexans. While particularly prevalent in amphibians and reptiles, the genus is more well known in veterinary circles for causing a tick-borne disease called hepatozoonosis in some mammals.
A canine vector-borne disease (CVBD) is one of "a group of globally distributed and rapidly spreading illnesses that are caused by a range of pathogens transmitted by arthropods including ticks, fleas, mosquitoes and phlebotomine sandflies." CVBDs are important in the fields of veterinary medicine, animal welfare, and public health. Some CVBDs are of zoonotic concern.
Anaplasmosis is a tick-borne disease affecting ruminants, dogs, and horses, and is caused by Anaplasma bacteria. Anaplasmosis is an infectious but not contagious disease. Anaplasmosis can be transmitted through mechanical and biological vector processes. Anaplasmosis can also be referred to as "yellow bag" or "yellow fever" because the infected animal can develop a jaundiced look. Other signs of infection include weight loss, diarrhea, paleness of the skin, aggressive behavior, and high fever.
Babesia divergens is an intraerythrocytic parasite, transmitted by the tick Ixodes ricinus. It is the most common cause of human babesiosis. It is the main agent of bovine babesiosis, or "redwater fever", in Europe. Young cattle are less susceptible. The current emphasis in Europe on sustainable agriculture and extensification is likely to lead to an increase in vector tick populations with increased risk of infection. B. divergens is also prevalent in cottontail rabbits on Nantucket Island, Massachusetts, USA.
Ixodes scapularis is commonly known as the deer tick or black-legged tick, and in some parts of the US as the bear tick. It was also named Ixodes dammini until it was shown to be the same species in 1993. It is a hard-bodied tick found in the eastern and northern Midwest of the United States as well as in southeastern Canada. It is a vector for several diseases of animals, including humans and is known as the deer tick owing to its habit of parasitizing the white-tailed deer. It is also known to parasitize mice, lizards, migratory birds, etc. especially while the tick is in the larval or nymphal stage.
Theileria is a genus of parasites that belongs to the phylum Apicomplexa, and is closely related to Plasmodium. Two Theileria species, T. annulata and T. parva, are important cattle parasites. T. annulata causes tropical theileriosis and T. parva causes East Coast fever. Theileria species are transmitted by ticks. The genomes of T. orientalis Shintoku, Theileria equi WA, Theileria annulata Ankara and Theileria parva Muguga have been sequenced and published.
Babesia microti is a parasitic blood-borne piroplasm transmitted by deer ticks. B. microti is responsible for the disease babesiosis, a malaria-like disease which also causes fever and hemolysis.
Piroplasmida is an order of parasites in the phylum Apicomplexa. They divide by binary fission and as sporozoan parasites they possess sexual and asexual phases. They include the tick parasites Babesia and Theileria.
Rhipicephalus sanguineus, commonly called the brown dog tick, kennel tick, or pantropical dog tick, is a species of tick found worldwide, but more commonly in warmer climates. This species is unusual among ticks in that its entire lifecycle can be completed indoors. The brown dog tick is easily recognized by its reddish-brown color, elongated body shape, and hexagonal basis capituli. Adults are 2.28 to 3.18 mm in length and 1.11 to 1.68 mm in width. They do not have ornamentation on their backs.
Hematozoa is a subclass of blood parasites of the Apicomplexa clade. Well known examples include the Plasmodium spp. which cause malaria in humans and Theileria which causes theileriosis in cattle. A large number of species are known to infect birds and are transmitted by insect vectors. The pattern in which Haematozoa infect a host cell depends on the genera of the blood parasite. Plasmodium and Leucozytozoon displace the nucleus of the host cell so that the parasite can take control of the cell where as Hemoproteus completely envelops the nucleus in a host cell.
Babesia bovis is an Apicomplexan single-celled parasite of cattle which occasionally infects humans. The disease it and other members of the genus Babesia cause is a hemolytic anemia known as babesiosis and colloquially called Texas cattle fever, redwater or piroplasmosis. It is transmitted by bites from infected larval ticks of the order Ixodida. It was eradicated from the United States by 1943, but is still present in Mexico and much of the world's tropics. The chief vector of Babesia species is the southern cattle fever tick Rhipicephalus microplus.
Theileria parva is a species of parasites, named in honour of Arnold Theiler, that causes East Coast fever (theileriosis) in cattle, a costly disease in Africa. The main vector for T. parva is the tick Rhipicephalus appendiculatus. Theiler found that East Coast fever was not the same as redwater, but caused by a different protozoan.
Ornithodoros moubata, commonly known as the African hut tampan or the eyeless tampan, is a species of tick in the family Argasidae. It is an ectoparasite and vector of relapsing fever in humans, and African swine fever in pigs.
Xenodiagnosis is a diagnostic method used to document the presence of infectious disease microorganisms or pathogens by exposing possibly infected tissue to a vector and then examining the vector for the presence of the microorganisms or pathogens it may have ingested.
Achromatorida is an order of non-pigmented intraerythrocytic parasitic alveolates belonging to the subclass Haemosporidiasina. The order was created by Jacques Euzéby in 1988.
Ticks of domestic animals directly cause poor health and loss of production to their hosts. Ticks also transmit numerous kinds of viruses, bacteria, and protozoa between domestic animals. These microbes cause diseases which can be severely debilitating or fatal to domestic animals, and may also affect humans. Ticks are especially important to domestic animals in tropical and subtropical countries, where the warm climate enables many species to flourish. Also, the large populations of wild animals in warm countries provide a reservoir of ticks and infective microbes that spread to domestic animals. Farmers of livestock animals use many methods to control ticks, and related treatments are used to reduce infestation of companion animals.
Babesia canis is a parasite that infects red blood cells and can lead to anemia. This is a species that falls under the overarching genus Babesia. It is transmitted by the brown dog tick and is one of the most common piroplasm infections. The brown dog tick is adapted to warmer climates and is found in both Europe and the United States, especially in shelters and greyhound kennels. In Europe, it is also transmitted by Dermacentor ticks with an increase in infections reported due to people traveling with their pets.
Rhipicephalus haemaphysaloides is a hard-bodied tick of the genus Rhipicephalus. It is one of the major medically important ticks in the world.
References
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↑ Khayat A, Rathore M (2008). "Ch. 36: Babesia Species". In Barton LL, Volpe JJ, Friedman NR (eds.). The Neurological Manifestations of Pediatric Infectious Diseases and Immunodeficiency Syndromes. Humana Press. pp.343–6. ISBN978-1-59745-391-2.
1 2 Randolph, S. E. (2004). "Evidence that climate change has caused 'emergence' of tick-borne diseases in Europe?". International Journal of Medical Microbiology. 293: 5–15. doi:10.1016/s1433-1128(04)80004-4. PMID15146980.
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↑ Peirce M (June 1975). "Nuttallia França, 1909 (babesiidae) preoccupied by Nuttallia Dall, 1898 (psammobiidae): A re-appraisal of the taxonomic position of the avian piroplasms". International Journal for Parasitology. 5 (3): 285–287. doi:10.1016/0020-7519(75)90075-2. ISSN0020-7519. PMID1126783.
↑ Earlé RA, Huchzermeyer FW, Bennett GF, Brossy JJ (January 1993). "Babesia peirceisp. nov. from the jackass penguin". South African Journal of Zoology. 28 (2): 88–90. doi:10.1080/02541858.1993.11448298. ISSN0254-1858.
1 2 Merino S (April 1998). "Babesia bennetti n. sp. from the Yellow-Legged Gull (Larus cachinnans, Aves, Laridae) on Benidorm Island, Mediterranean Sea". The Journal of Parasitology. 84 (2): 422–424. doi:10.2307/3284504. ISSN0022-3395. JSTOR3284504. PMID9576519.
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