Multiple-locus variable-number tandem repeat analysis potentially reveals the existence of two groups of Anaplasma phagocytophilum circulating in cattle in France with different wild reservoirs

Abstract

Background Anaplasma phagocytophilum is the causative agent of tick-borne fever, a disease with high economic impact for domestic ruminants in Europe. Epidemiological cycles of this species are complex, and involve different ecotypes circulating in various host species. To date, these epidemiological cycles are poorly understood, especially in Europe, as European reservoir hosts (i.e. vertebrate hosts enabling long-term maintenance of the bacterium in the ecosystem), of the bacterium have not yet been clearly identified. In this study, our objective was to explore the presence, the prevalence, and the genetic diversity of A. phagocytophilum in wild animals, in order to better understand their implications as reservoir hosts of this pathogen.MethodsThe spleens of 101 wild animals were collected from central France and tested for the presence of A. phagocytophilum DNA by msp2 qPCR. Positive samples were then typed by multi-locus variable-number tandem repeat (VNTR) analysis (MLVA), and compared to 179 previously typed A. phagocytophilum samples.Results Anaplasma phagocytophilum DNA was detected in 82/101 (81.2%) animals including 48/49 red deer (98%), 20/21 roe deer (95.2%), 13/29 wild boars (44.8%), and 1/1 red fox. MLVA enabled the discrimination of two A. phagocytophilum groups: group A contained the majority of A. phagocytophilum from red deer and two thirds of those from cattle, while group B included a human strain and variants from diverse animal species, i.e. sheep, dogs, a horse, the majority of variants from roe deer, and the remaining variants from cattle and red deer.ConclusionsOur results suggest that red deer and roe deer are promising A. phagocytophilum reservoir host candidates. Moreover, we also showed that A. phagocytophilum potentially circulates in at least two epidemiological cycles in French cattle. The first cycle may involve red deer as reservoir hosts and cattle as accidental hosts for Group A strains, whereas the second cycle could involve roe deer as reservoir hosts and at least domestic ruminants, dogs, horses, and humans as accidental hosts for Group B strains.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1888-4) contains supplementary material, which is available to authorized users.

The Occurrence of Zoonotic Anaplasma phagocytophilum Strains, in the Spleen and Liver of Wild Boars from North-West and Central Parts of Poland

“…The prevalence of Anaplasma phagocytophilum in wild boars varies across Europe and elsewhere, ranging from 0.97% in Belgium [ 24 ] to 44.8% in France [ 13 ]. In addition, one study reports that genetic material of A. phagocytophilum was not detected in the tested wild boar in Slovakia [ 25 ].…”

“…Many wild animals, such as roe deer ( Capreolus capreolus ), red deer ( Cervus elaphus ), wild boar ( Sus scrofa ), red fox ( Vulpes vulpes ), raccoon dog ( Nyctereutes procyonoides ) and the European badger ( Meles meles ) are infected with A. phagocytophilum [ 11 , 12 ]. Wild boars are likely to be natural wild reservoir hosts for potentially zoonotic A. phagocytophilum strains; however, there is still little data to confirm this statement [ 11 , 13 ].…”

Detecting and characterizing mixed infections with genetic variants of Anaplasma phagocytophilum in roe deer (Capreolus capreolus) by developing an ankA cluster-specific nested PCR

“…We found in France an overall prevalence of 52.3% when the three geographical sites are considered. Prevalences of 78 and 95.2% were reported in south-west France and central France, respectively, after qPCR of the msp2 or p44 gene [ 24 , 30 ]. Our results confirm the role of roe deer as an important natural reservoir of A. phagocytophilum .…”

“…Vertebrate hosts are considered to serve as critical reservoirs in the life-cycle of A. phagocytophilum , since transovarial transmission may occur in Ixodes tick species, but at a low level [ 9 , 23 ]. Whether roe deer are involved in epidemiological cycles likely to involve the infection (even accidental) of humans or livestock remains to be clarified [ 7 , 24 ]. In roe deer, prevalences of A. phagocytophilum higher than 70% have been reported in several European countries (Germany, France, Slovenia and Austria) [ 6 , 24 – 28 ].…”

“…Whether roe deer are involved in epidemiological cycles likely to involve the infection (even accidental) of humans or livestock remains to be clarified [ 7 , 24 ]. In roe deer, prevalences of A. phagocytophilum higher than 70% have been reported in several European countries (Germany, France, Slovenia and Austria) [ 6 , 24 – 28 ]. With such high prevalences, co-infections or superinfections are therefore likely to occur [ 29 ].…”