The natural history of Anaplasma marginale

doi:10.1016/j.vetpar.2009.09.012

Veterinary Parasitology

Volume 167, Issues 2–4, 10 February 2010, Pages 95-107

https://doi.org/10.1016/j.vetpar.2009.09.012 Get rights and content

Abstract

The intracellular pathogen Anaplasma marginale (Rickettsiales: Anaplasmataceae), described by Sir Arnold Theiler in 1910, is endemic worldwide in tropical and subtropical areas. Infection of cattle with A. marginale causes bovine anaplasmosis, a mild to severe hemolytic disease that results in considerable economic loss to both dairy and beef industries. Transmission of A. marginale to cattle occurs biologically by ticks and mechanically by biting flies and by blood-contaminated fomites. Both male ticks and cattle hosts become persistently infected with A. marginale and serve as reservoirs of infection. While erythrocytes are the major site of infection in cattle, A. marginale undergoes a complex developmental cycle in ticks that begins by infection of gut cells, and transmission to susceptible hosts occurs from salivary glands during feeding. Major surface proteins (MSPs) play a crucial role in the interaction of A. marginale with host cells, and include adhesion proteins and MSPs from multigene families that undergo antigenic change and selection in cattle, thus contributing to maintenance of persistent infections. Many geographic strains of A. marginale have been identified worldwide, which vary in genotype, antigenic composition, morphology and infectivity for ticks. Isolates of A. marginale may be maintained by independent transmission events and a mechanism of infection/exclusion in cattle and ticks. The increasing numbers of A. marginale genotypes identified in some geographic regions most likely resulted from intensive cattle movement. However, concurrent A. marginale strain infections in cattle was reported, but these strains were more distantly related. Phylogenetic studies of selected geographic isolates of A. marginale, using msp4 and msp1α, provided information about the biogeography and evolution of A. marginale, and msp1α genotypes appear to have evolved under positive selection pressure. Live and killed vaccines have been used for control of anaplasmosis and both types of vaccines have advantages and disadvantages. Vaccines have effectively prevented clinical anaplasmosis in cattle but have failed to block A. marginale infection. Vaccines are needed that can prevent clinical disease and, simultaneously, prevent infection in cattle and ticks, thus eliminating these hosts as reservoirs of infection. Advances in genomics, proteomics, immunology and biochemical and molecular technologies during the last decade have been applied to research on A. marginale and related organisms, and the recent development of a cell culture system for A. marginale has provided a format for studying the pathogen/tick interface. Recent advancements and new research methodologies should provide additional opportunities for development of new strategies for control and prevention of bovine anaplasmosis.

Section snippets

Historical background

The genus Anaplasma was erected in 1910 by Sir Arnold Theiler who first recognized that “marginal points” found in stained erythrocytes of sick cattle were the causative agent of a specific disease (Theiler, 1910a, Theiler, 1910b, Theiler, 1911). Publishing from his station in South Africa, he dubbed the type species of the newly created genus, which he tentatively concluded was a protozoan, Anaplasma marginale. The marginally located inclusions had been seen frequently in red blood cells of

Epidemiology

Bovine anaplasmosis occurs in tropical and subtropical areas throughout the world and the disease is a major constraint to cattle production in many countries. A. marginale, in contrast to Anaplasma phagocytophilum, is quite host specific, infecting only ruminants and causing disease primarily in cattle. In the U.S.A. anaplasmosis is enzootic throughout the southern Atlantic states, Gulf Coast states, and several of the Midwestern and Western states (McCallon, 1973). However, anaplasmosis has

Transmission and arthropod vectors

Transmission of A. marginale can be effected both mechanically by biting flies or blood-contaminated fomites and biologically by ticks (Dikmans, 1950, Kocan, 1986, Kocan et al., 2003, Kocan et al., 2004a). Recent research documented that biological transmission by ticks was more efficient than mechanical transmission by Stomoxys calcitrans, the stable fly (Scoles et al., 2005a). However, some strains of A. marginale are not infective for or transmissible by ticks (as reviewed by Kocan et al.,

Reservoir hosts

Clinical anaplasmosis occurs most often in cattle, but other ruminants including water buffalo (Bubalus bubalis), American bison (Bison bison), white-tailed deer (Odocoileus virginianus), mule deer (Odocoileus hemionus hemionus), black-tailed deer (Odocoileus hemionus columbianus) and Rocky Mountain elk (Cervus elaphus nelsoni) can become infected with A. marginale (reviewed by Kuttler, 1984, Zaugg et al., 1996). Wild ruminants, particularly mule deer and elk, may be implicated in the

Taxonomy, phylogeny and genomics

Organisms assigned to the Order Rickettsiales were recently reclassified. The reclassification was based upon genetic analyses of 16S rRNA genes, groESL and surface protein genes (Dumler et al., 2001), and organisms were assigned to one of two families: Anaplasmataceae and Rickettsiaceae. Among the Anaplasmactaceae, the phylogenetic analyses consistently supported formation of four genetically distinct groups: (1) Anaplasma with a 96.1% minimum similarity, (2) Ehrlichia (97.7% similarity), (3)

Agent and developmental cycle

Sir Arnold Theiler first described A. marginale infection in erythrocytes of South African cattle as “marginal points” (Theiler, 1910b). A similar report was published in the U.S.A. by Salmon and Smith in 1896 which described the presence of a point-like pathogen in blood smears of cattle as “…[a] very minute roundish body which is stained blue to bring it into view. The body as a rule is situated near the edge of the corpuscle” (Salmon and Smith, 1896). Theiler subsequently described a

Culture

Short-term propagation of the erythrocytic stage of A. marginale in various culture systems enabled study of A. marginale outside of cattle or ticks (Kessler et al., 1979, Kessler and Ristic, 1979, Mazzola and Kuttler, 1980; as reviewed by Blouin et al., 2002). Kessler et al. (1979) established a whole-blood culture of A. marginale based on a method used to cultivate Plasmodium. The viability of the organism in erythrocytes was demonstrated by inoculation of susceptible calves with blood

Clinical diagnosis

A diagnosis of bovine anaplasmosis may be made tentatively based on geographic location, season, signalment and presenting clinical signs and/or necropsy findings observed in infected animals (Jones and Brock, 1966). In order to confirm the diagnosis, laboratory tests such as light microscopic evaluation of stained blood smears or serological/molecular diagnostic procedures are required. The latter are the only means of identifying persistently infected, subclinical carrier cattle. Producers in

Immunopathology

Bovine anaplasmosis often results in development of mild to severe anemia and icterus without hemoglobinemia and hemoglobinuria. Clinical symptoms may include fever, weight loss, abortion, lethargy, icterus, and often death in animals over 2 years old (reviewed by Kocan et al., 2003, Kocan et al., 2004a). Cattle that survive acute infection develop persistent infections characterized by cyclic low level rickettsemia (Kieser et al., 1990). Recent research, as reviewed by Palmer (1989), and

Treatment, prevention and control

Control measures for anaplasmosis have not changed markedly over the past 60 years. Measures vary with geographic location and include arthropod control by application of acaricides, prophylactic administration of antibiotics, and vaccination. Arthropod control is not practical in many areas and can only partially protect against A. marginale transmission, which often occurs by mechanical transmission of infected blood by fomites. Chemotherapy, probably used more often for prevention of

Conclusions

A. marginale, which is endemic in tropical, subtropical and certain temperate areas of the world, is a challenging pathogen to study. A. marginale is quite host specific for ruminants, and anaplasmosis occurs primarily in cattle; certain other ruminants may serve as reservoirs of infection. While A. marginale is transmitted biologically by ticks, mechanical transmission by blood-contaminated mouthparts of biting flies or fomites also frequently occurs. Mechanical transmission may be the only

Conflict of interest

None declared.

Acknowledgments

This research was supported by the project No. 1669 of the Oklahoma Agricultural Experiment Station, the Sitlington Endowed Chair for Food Animal Research (K.M. Kocan) and the Instituto de Ciencias de la Salud, Spain (ICS-JCCM) (project 03052-00).

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ReviewThe natural history of Anaplasma marginale

Abstract

Section snippets

Historical background

Epidemiology

Transmission and arthropod vectors

Reservoir hosts

Taxonomy, phylogeny and genomics

Agent and developmental cycle

Culture

Clinical diagnosis

Immunopathology

Treatment, prevention and control

Conclusions

Conflict of interest

Acknowledgments

Res. Vet. Sci.

Vet. Parasitol.

Vet. Microbiol.

Vet. Microbiol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Microbiol.

Vet. Microbiol.

Vet. Microbiol.

Parasitol. Today

Vet. Parasitol.

Vet. J.

Vet. Parasitol.

Res. Vet. Sci.

Vet. Microbiol.

Vet. Microbiol.

Frozen and fresh Anaplasma centrale vaccines in the protection of cattle against Anaplasma marginale infection

Rev. Élev. Méd. Vet. Pays Trop.

Genetic diversity of Anaplasma marginale strains from an acute bovine anaplasmosis outbreak within a herd in an endemic area

Vet. Parasitol.

Fluoroquinolones, mechanism of action, classification and development of resistance

Survey Ophthamol.

Morphology and development of Anaplasma marginale (Rickettsiales: Anaplasmatacea) in cultured Ixodes scapularis (Acari: Ixodidae) cells

J. Med. Entomol.

Effect of 4-bromo-calcium ionophore A23187 on the release of Anaplasma marginale from bovine erythrocytes in vitro

Am. J. Vet. Res.

Applications of a cell culture system for studying the interaction of Anaplasma marginale with tick cells

Anim. Health Res. Rev.

Immunity following use of Australian tick fever vaccine: a review of the evidence

Aust. Vet. J.

Anaplasmosis: control of the first outbreak in Canada by serologic identification and slaughter

Can. J. Comp. Med.

Deer as carriers of anaplasmosis

Science

Sensitivity and specificity of the complement fixation test for detection of cattle persistently infected with Anaplasma marginale

J. Vet. Diagn. Invest.

Complete genome sequencing of Anaplasma marginale reveals that the surface is skewed to two superfamilies of outer membrane proteins

Proc. Natl. Acad. Sci. U.S.A.

Anaplasmosis control by test and subsequent treatment with chlortetracycline

A vaccine for anaplasmosis

J. Am. Vet. Med. Assoc.

CD4+ T-lymphocyte and immunoglobulin G2 responses in calves immunized with Anaplasma marginale outer membranes and protected against homologous challenge

Infect. Immun.

Antibody prevalence of eight ruminant infectious diseases in California mule and black-tailed deer (Odocoileus hemionus)

J. Wildlife Dis.

Comparison of three oxytetracycline regimens for the treatment of persistent Anaplasma marginale infections in beef cattle

Vet. Parasitol.

Flow cytometric evaluation of selected antimicrobial efficacy for clearance of Anaplasma marginale in short-term erythrocyte cultures

J. Vet. Pharmacol. Ther.

Efficacy of enrofloxacin against severe experimental Anaplasma marginale infections in splenectomized calves

Vet. Ther.

Anaplasmosis in cattle (Galziete) found to exist in Kansas

N. Am. Vet.

Synthesis of DNA and protein by Anaplasma marginale in bovine erythrocytes during short-term culture

Infect. Immun.

Evolution and function of tandem repeats in the major surface protein 1a of the ehrlichial pathogen Anaplasma marginale

Anim. Health Res. Rev.

Infection of tick cells and bovine erythrocytes with one genotype of the intracellular ehrlichia Anaplasma marginale excludes infection with other genotypes

Clin. Diagn. Lab. Immunol.

Characterization of Anaplasma marginale isolated from North American bison

Appl. Environ. Microbiol.

Infection exclusion of the rickettsial pathogen, Anaplasma marginale, in the tick vector, Dermacentor variabilis

Clin. Diagn. Lab. Immunol.

Anaplasma marginale major surface protein 1α genotypes evolved under positive selection pressure but are not a marker for geographic isolates

Review
The natural history of Anaplasma marginale

CD4⁺ T-lymphocyte and immunoglobulin G2 responses in calves immunized with Anaplasma marginale outer membranes and protected against homologous challenge