Simultaneous infection of cattle with different Anaplasma phagocytophilum variants

Tegtmeyer, P. C.; Ganter, Martin; Loewenich, Friederike D. von

doi:10.1016/j.ttbdis.2019.05.011

Cited by 11 publications

(12 citation statements)

References 38 publications

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“…However, an A. phagocytophilum strain from a water buffalo with typical signs of tick-borne fever was also found in the roe-deer-associated MLST and ankA gene Cluster 2 [22]. On the other hand, 98% (62/63) available bovine housekeeping gene sequences from this and previous studies [16,26] were part of MLST Cluster 1. Further, 82% (58/71) of the ankA sequences from cattle were found in ankA Cluster 1 and 17% (12/71) in Cluster 4.…”

Section: Discussionsupporting

confidence: 41%

“…The concept of co-infection with different A. phagocytophilum variants is supported by the fact that 41% (14/34) of I. ricinus ticks were infected with more than one ST [16]. Further, naturally infected cattle simultaneously harbored more than one A. phagocytophilum variant because double peaks were observed in the chromatograms of the genetic loci investigated [26,29]. However, most animals were only sampled once, or the full profile of all loci was not available in these studies.…”

Section: Discussionmentioning

confidence: 99%

“…The concatenated housekeeping gene sequences from our study were compared to 347 sequences without ambiguous nucleotides described previously [16,22,[24][25][26]. The sequences were found in six clusters (Additional file 4: Fig.…”

Section: Comparison To Previously Published Housekeeping Gene Sequencesmentioning

confidence: 99%

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Co-infection, reinfection and superinfection with Anaplasma phagocytophilum strains in a cattle herd based on ankA gene and multilocus sequence typing

et al. 2020

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Background: Anaplasma phagocytophilum is a Gram-negative obligate intracellular bacterium that replicates in neutrophil granulocytes. It is transmitted by ticks of the Ixodes ricinus complex and causes febrile illness in humans and animals. We used multilocus sequence typing (MLST) and ankA gene-based typing to study the molecular epidemiology of the A. phagocytophilum strains circulating in a German cattle herd over one pasture season. The aim was to investigate whether co-infection with two distinct variants, reinfection with the same and/or superinfection by a different strain occurred during one pasture season. Eight genetic loci were sequenced in 47 PCR-positive samples from 15 animals. Results: Five different sequence types (ST) and four ankA alleles were detected in the cattle herd. Three different ST caused clinically overt tick-borne fever in primary infected animals. The concordance between ST and ankA allele was 100%. Therefore, the housekeeping genes used for MLST and the highly variable ankA gene were concatenated to increase resolution. Co-infection could be proven because samples of chronologically close collection dates were included. Co-infecting A. phagocytophilum strains differed by 14 to 18 single nucleotide polymorphisms (SNPs). Most superinfecting variants varied by 14 SNPs from the previous strain and appeared in median after a free interval of 31 days. Thus, it is unlikely that superinfecting strains arose by in-animal evolution. Immunity against re-or superinfection was assumed because the cattle developed clinical signs only during primary infection. Conclusions: The tick-pathogen-vertebrate host interaction is probably much more complex than previously thought taking into account the frequently occurring events of co-infection, reinfection and superinfection. This complex situation could not be easily simulated in an experimental infection and underlines the value of field studies.

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Section: Discussionsupporting

confidence: 41%

Section: Discussionmentioning

confidence: 99%

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Co-infection, reinfection and superinfection with Anaplasma phagocytophilum strains in a cattle herd based on ankA gene and multilocus sequence typing

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“…In total, about 7% of ticks (nymphs as well as adults) from the two types of sites harbored both ecotype I and II, suggesting that either the ticks fed on hosts co-infected with different A. phagocytophilum strains or larvae and nymphs fed successively on hosts harboring various strains. Simultaneous infection of vertebrates with multiple A. phagocytophilum strains was found to exist and has recently been confirmed, for example, for roe deer from France that harbored 2–3 ankA gene variants [15] or cattle from Germany infected with two ankA variants and multiple MLST sequence types [44]. Co-infections may lead to bacterial recombination and emergence of new genetic variants [44,45].…”

Section: Discussionmentioning

confidence: 99%

Presence of Roe Deer Affects the Occurrence of Anaplasma phagocytophilum Ecotypes in Questing Ixodes ricinus in Different Habitat Types of Central Europe

Hamšíková

Silaghi

Takumi

et al. 2019

IJERPH

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The way in which European genetic variants of Anaplasma phagocytophilum circulate in their natural foci and which variants cause disease in humans or livestock remains thus far unclear. Red deer and roe deer are suggested to be reservoirs for some European A. phagocytophilum strains, and Ixodes ricinus is their principal vector. Based on groEL gene sequences, five A. phagocytophilum ecotypes have been identified. Ecotype I is associated with the broadest host range, including strains that cause disease in domestic animals and humans. Ecotype II is associated with roe deer and does not include zoonotic strains. In the present study, questing I. ricinus were collected in urban, pasture, and natural habitats in the Czech Republic, Germany, and Slovakia. A fragment of the msp2 gene of A. phagocytophilum was amplified by real-time PCR in DNA isolated from ticks. Positive samples were further analyzed by nested PCRs targeting fragments of the 16S rRNA and groEL genes, followed by sequencing. Samples were stratified according to the presence/absence of roe deer at the sampling sites. Geographic origin, habitat, and tick stage were also considered. The probability that A. phagocytophilum is a particular ecotype was estimated by a generalized linear model. Anaplasma phagocytophilum was identified by genetic typing in 274 I. ricinus ticks. The majority belonged to ecotype I (63.9%), 28.5% were ecotype II, and both ecotypes were identified in 7.7% of ticks. Ecotype II was more frequently identified in ticks originating from a site with presence of roe deer, whereas ecotype I was more frequent in adult ticks than in nymphs. Models taking into account the country-specific, site-specific, and habitat-specific aspects did not improve the goodness of the fit. Thus, roe deer presence in a certain site and the tick developmental stage are suggested to be the two factors consistently influencing the occurrence of a particular A. phagocytophilum ecotype in a positive I. ricinus tick.

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“…In I. ricinus, R. helvetica, R. monacensis, R. massiliae and R. felis have been detected, with R. helvetica being the most frequent [3][4][5][6][7]. Another member of the order Rickettsiales, A. phagocytophilum, may cause granulocytic anaplasmosis in humans, dogs, horses, goats, sheep and cattle [8][9][10].…”

Section: Introductionmentioning

confidence: 99%

Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae

et al. 2020

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Background: Ixodes ricinus constitutes the main European vector tick for the Lyme borreliosis pathogen Borrelia burgdorferi (sensu lato), the relapsing fever borrelia Borrelia miyamotoi, as well as Anaplasma phagocytophilum and several Rickettsia species. Under laboratory conditions, a transovarial transmission to the next tick generation is described for Rickettsia spp. and Borrelia spp., especially regarding B. miyamotoi, whereas the efficiency of transovarial transfer under field conditions is largely unstudied. Methods: In order to better estimate the potential infection risk by tick larvae for humans and animals, 1500 I. ricinus larvae from 50 collected "nests" (larvae adhering to the flag in a clumped manner) were individually examined for Borrelia, Rickettsia and A. phagocytophilum DNA using quantitative real-time PCR (qPCR). Results: Thirty-nine of 50 nests each (78.0%, 95% CI: 64.0-88.5%) were positive for Borrelia spp. and Rickettsia spp. DNA, and in three nests (6.0%, 95% CI: 1.3-16.5%) A. phagocytophilum DNA was detected. Overall, DNA from at least one pathogen could be detected in 90.0% (45/50, 95% CI: 78.2-96.7%) of the nests. Of the 1500 larvae, 137 were positive for Borrelia spp. DNA (9.1%, 95% CI: 7.7-10.7%), 341 for Rickettsia spp. DNA (22.7%, 95% CI: 20.6-24.9%) and three for A. phagocytophilum DNA (0.2%, 95% CI: 0-0.6%). Quantity of Borrelia spp. and Anaplasma spp. DNA in positive larvae was low, with 2.7 × 10 0 Borrelia 5S-23S gene copies and 2.4 × 10 1 A. phagocytophilum msp2/p44 gene copies detected on average, while Rickettsia-positive samples contained on average 5.4 × 10 2 gltA gene copies. Coinfections were found in 66.0% (33/50, 95% CI: 51.2-78.8%) of the nests and 8.6% (38/443, 95% CI: 6.1-11.6%) of positive larvae. In fact, larvae had a significantly higher probability of being infected with Borrelia spp. or Rickettsia spp. when both pathogens were present in the nest. Conclusions: This study provides evidence for transovarial transmission of Rickettsia spp. and Borrelia spp. in I. ricinus under field conditions, possibly facilitating pathogen persistence in the ecosystem and reducing the dependence on

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Simultaneous infection of cattle with different Anaplasma phagocytophilum variants

Cited by 11 publications

References 38 publications

Co-infection, reinfection and superinfection with Anaplasma phagocytophilum strains in a cattle herd based on ankA gene and multilocus sequence typing

Co-infection, reinfection and superinfection with Anaplasma phagocytophilum strains in a cattle herd based on ankA gene and multilocus sequence typing

Presence of Roe Deer Affects the Occurrence of Anaplasma phagocytophilum Ecotypes in Questing Ixodes ricinus in Different Habitat Types of Central Europe

Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae

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