Identification of Midgut and Salivary Glands as Specific and Distinct Barriers to Efficient Tick-Borne Transmission of<i>Anaplasma marginale</i>

Ueti, Massaro W.; Reagan, J. O.; Knowles, Donald P.; Scoles, Glen A.; Shkap, Varda; Palmer, Guy H.

doi:10.1128/iai.00284-07

Cited by 78 publications

(128 citation statements)

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“…(Uilenberg, 1995;De Waal et al, 2000;Jongejan and Uilenberg, 2004;Kocan et al, 2004). Tick transmissibility of Anaplasma is complex and ranges from very efficient transmission to non-transmission related to both Anaplasma strains as well as species of tick (Ueti et al, 2007). In Morocco, the vector competency of local tick species for transmitting A. marginale has yet to be demonstrated.…”

Section: Introductionmentioning

confidence: 99%

Molecular and serological prevalence of Anaplasma marginale in cattle of North Central Morocco

Hamou

Rahali

Sahibi

et al. 2012

Research in Veterinary Science

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Section: Introductionmentioning

confidence: 99%

Molecular and serological prevalence of Anaplasma marginale in cattle of North Central Morocco

Hamou

Rahali

Sahibi

et al. 2012

Research in Veterinary Science

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“…While the A. marginale subsp. centrale vaccine strain was thought for a long time not to be transmitted by most ticks, it was shown that, in fact, it colonized the tick well but was not secreted into the tick saliva in sufficient quantities for robust transmission (23,24). Dramatically increasing tick numbers in transmission experiments overcame the transmission barrier (25).…”

Section: Discussionmentioning

confidence: 99%

Characterization of Anaplasma marginale subsp. centrale Strains by Use of msp1aS Genotyping Reveals a Wildlife Reservoir

et al. 2016

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Bovine anaplasmosis caused by the intraerythrocytic rickettsial pathogen Anaplasma marginale is endemic in South Africa. Anaplasma marginale subspecies centrale also infects cattle; however, it causes a milder form of anaplasmosis and is used as a live vaccine against A. marginale. There has been less interest in the epidemiology of A. marginale subsp. centrale, and, as a result, there are few reports detecting natural infections of this organism. When detected in cattle, it is often assumed that it is due to vaccination, and in most cases, it is reported as coinfection with A. marginale without characterization of the strain. A total of 380 blood samples from wild ruminant species and cattle collected from biobanks, national parks, and other regions of South Africa were used in duplex real-time PCR assays to simultaneously detect A. marginale and A. marginale subsp. centrale. PCR results indicated high occurrence of A. marginale subsp. centrale infections, ranging from 25 to 100% in national parks. Samples positive for A. marginale subsp. centrale were further characterized using the msp1aS gene, a homolog of msp1␣ of A. marginale, which contains repeats at the 5= ends that are useful for genotyping strains. A total of 47 Msp1aS repeats were identified, which corresponded to 32 A. marginale subsp. centrale genotypes detected in cattle, buffalo, and wildebeest. RepeatAnalyzer was used to examine strain diversity. Our results demonstrate a diversity of A. marginale subsp. centrale strains from cattle and wildlife hosts from South Africa and indicate the utility of msp1aS as a genotypic marker for A. marginale subsp. centrale strain diversity. Bovine anaplasmosis (gallsickness) is a tick-borne disease caused by the intraerythrocytic rickettsial pathogen Anaplasma marginale (1). A. marginale is globally prevalent and results in anemia, with mortality rates of up to 30% (2). Anaplasma marginale subspecies centrale is a less virulent subspecies detected by Sir Arnold Theiler, who recognized its potential as a vaccine against anaplasmosis; 100 years later this live vaccine is still in use in South Africa, Israel, South America, and Australia (3, 4). The strain that is used as a vaccine originated from Theiler's original isolation and was exported at various times to other countries where it has been propagated in the laboratory; the strain known as the "Israel strain" or the "vaccine strain" was sent to Israel in the 1950s and was used to generate the complete genome sequence for A. marginale subsp. centrale in 2010 (5). A. marginale subsp. centrale does not provide complete protection against A. marginale infection but does protect against severe anaplasmosis (6, 7). (8)(9)(10)(11). Cattle are naturally susceptible to A. marginale (4). There has not been much interest in the epidemiology of A. marginale subsp. centrale, with few reports detecting natural infections of this organism; most often, when detected in cattle it is assumed that it is due to vaccination and is reported as coinfection with A. marginale without...

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“…The initial infection and a first round of intracellular replication occur within the tick midgut epithelium (7,9,10). The ability to enter and replicate in the midgut epithelium has been shown to be a determinant of A. marginale strain transmission fitness in the tick Dermacentor andersoni (16). Whether simultaneous acquisition of two A. marginale strains results in competition between the strains has not been tested, but entry of a first A. marginale strain into the midgut has been postulated to prevent establishment of infection by a second strain via a process termed "infection exclusion" (3).…”

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Tick-Borne Transmission of Two Genetically DistinctAnaplasma marginaleStrains following Superinfection of the Mammalian Reservoir Host

et al. 2008

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Strain superinfection affects the dynamics of epidemiological spread of pathogens through a host population. Superinfection has recently been shown to occur for two genetically distinct strains of the tick-borne pathogen Anaplasma marginale that encode distinctly different surface protein variants. Superinfected animals could serve as a reservoir for onward transmission of both strains if the tick vector is capable of acquiring and transmitting both strains. Whether competition among strains during development within the tick vector, which requires sequential invasion and replication events, limits colonization and subsequent transmission to a single strain is unknown. We tested this possibility by acquisition feeding Dermacentor andersoni ticks on a reservoir host superinfected with the genetically distinct St. Maries and EM⌽ strains. Although the St. Maries strain consistently maintained higher bacteremia levels in the mammalian host and the EM⌽ strain had an early advantage in colonization of the tick salivary glands, individual ticks were coinfected, and there was successful transmission of both strains. These results indicate that a genetically distinct A. marginale strain capable of superinfecting the mammalian host can subsequently be cotransmitted and become established within the host population despite the presence of an existing established strain.Superinfection occurs when a second, genetically distinct pathogen strain infects a host already carrying a primary strain of the same pathogen species. Superinfection allows the second strain to become established in the host and compete with the primary strain for onward transmission. For antigenically variant microbial pathogens this requires that the second strain encode a unique set of variants. This hypothesis has recently been tested and accepted using the tick-borne bacterial pathogen Anaplasma marginale as a model (5). Strains of A. marginale that encode distinct variants of the immunodominant surface protein Msp2 are capable of superinfection despite the establishment of long-term infection and broad immunity against the variants encoded by the primary strain. Consequently, superinfected animals maintain an infection with two genetically distinct strains and, in theory, serve as reservoir hosts of both strains for subsequent tick transmission to naïve animals.Whether two distinct strains can be simultaneously acquired by the tick vector and subsequently transmitted is unknown, and this represents a gap in our knowledge that is relevant to pathogen strain structure in reservoir host populations. If only a single pathogen strain can be acquired and transmitted, then the new strain (either generated by genetic change or introduced) needs to have a significant competitive advantage to become established in the reservoir host population. Conversely, transmission of both strains to naïve animals would progressively expand the representation of the second strain in the population.A. marginale undergoes complex development within the tick, and pathogen str...

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Identification of Midgut and Salivary Glands as Specific and Distinct Barriers to Efficient Tick-Borne Transmission ofAnaplasma marginale

Cited by 78 publications

References 30 publications

Molecular and serological prevalence of Anaplasma marginale in cattle of North Central Morocco

Molecular and serological prevalence of Anaplasma marginale in cattle of North Central Morocco

Characterization of Anaplasma marginale subsp. centrale Strains by Use of msp1aS Genotyping Reveals a Wildlife Reservoir

Tick-Borne Transmission of Two Genetically DistinctAnaplasma marginaleStrains following Superinfection of the Mammalian Reservoir Host

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