Analyze Diet
Parasites & vectors2016; 9(1); 596; doi: 10.1186/s13071-016-1888-4

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: 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. The 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. 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. Our 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.
Publication Date: 2016-11-22 PubMed ID: 27876073PubMed Central: PMC5120488DOI: 10.1186/s13071-016-1888-4Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article explores the prevalence and genetic diversity of Anaplasma phagocytophilum, a bacterium causing tick-borne fever in cattle, in wild animals in France. It identifies two potential groups of the bacterium, suggesting a dual epidemiological cycle involving different animal reservoirs.

Research Aim and Methodology

  • This study aimed to understand better the presence, prevalence, and genetic diversity of Anaplasma phagocytophilum in wild animals. This understanding would help to identify their roles as reservoir hosts, i.e., vertebrate hosts facilitating the bacterium’s long-term preservation in the ecosystem.
  • The researchers collected spleens from 101 wild animals located in central France and tested them for the presence of A. phagocytophilum DNA using the msp2 qPCR method.
  • The positive samples were then differentiated by applying multi-locus variable-number tandem repeat (VNTR) analysis or MLVA.
  • The results from the MLVA were compared to 179 previously categorized A. phagocytophilum samples.

Key Findings

  • A. phagocytophilum DNA was discovered in 82 out of 101 animals. These included 98% of red deer, 95.2% of roe deer, 44.8% of wild boars, and a red fox.
  • MLVA helped to distinguish two A. phagocytophilum groups: Group A and Group B. Group A comprised most of the samples from red deer and two-thirds from cattle; while Group B had a human strain and variants from various animals like sheep, dogs, horse, most variants from roe deer, and remaining strains from cattle and red deer.
  • Based on these findings, red deer and roe deer are suggested as prospective A. phagocytophilum reservoir host candidates.
  • The research also indicates the existence of two potential epidemiological cycles in French cattle. The first may involve red deer as reservoir hosts and cattle as accidental hosts for Group A strains, while the second could involve roe deer as reservoir hosts and domestic ruminants, dogs, horses, and humans as accidental hosts for Group B strains.

Implications

  • This research enhances the understanding of the epidemiological cycles of A. phagocytophilum in Europe, specifically in France.
  • It could significantly help in developing strategies to control the spread of tick-borne fever.
  • By highlighting the potential role of different wild and domestic animals, the research could guide targeted interventions to reduce bacterium circulation.

Cite This Article

APA
Dugat T, Zanella G, Véran L, Lesage C, Girault G, Durand B, Lagrée AC, Boulouis HJ, Haddad N. (2016). 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. Parasit Vectors, 9(1), 596. https://doi.org/10.1186/s13071-016-1888-4

Publication

ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 9
Issue: 1
Pages: 596

Researcher Affiliations

Dugat, Thibaud
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail, Laboratoire de Santé Animale, UMR BIPAR, Université Paris-Est, Maisons-Alfort, France.
Zanella, Gina
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail, Laboratoire de Santé Animale, Unité d'Epidémiologie, Université Paris-Est, Maisons-Alfort, France.
Véran, Luc
  • Fédération des chasseurs du Loiret, Orléans, France.
Lesage, Céline
  • Fédération des chasseurs du Loiret, Orléans, France.
Girault, Guillaume
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail, Laboratoire de Santé Animale, Unité des Zoonoses Bactériennes, Université Paris-Est, Maisons-Alfort, France.
Durand, Benoît
  • Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail, Laboratoire de Santé Animale, Unité d'Epidémiologie, Université Paris-Est, Maisons-Alfort, France.
Lagrée, Anne-Claire
  • Ecole Nationale Vétérinaire d'Alfort, UMR BIPAR, Université Paris-Est, Maisons-Alfort, France.
Boulouis, Henri-Jean
  • Ecole Nationale Vétérinaire d'Alfort, UMR BIPAR, Université Paris-Est, Maisons-Alfort, France.
Haddad, Nadia
  • Ecole Nationale Vétérinaire d'Alfort, UMR BIPAR, Université Paris-Est, Maisons-Alfort, France. nadia.haddad@vet-alfort.fr.

MeSH Terms

  • Anaplasma phagocytophilum / classification
  • Anaplasma phagocytophilum / genetics
  • Anaplasma phagocytophilum / isolation & purification
  • Animals
  • Animals, Domestic
  • Cattle
  • Cattle Diseases / epidemiology
  • Cattle Diseases / microbiology
  • Deer
  • Ehrlichiosis / epidemiology
  • Ehrlichiosis / microbiology
  • Ehrlichiosis / veterinary
  • France / epidemiology
  • Genetic Variation
  • Genotype
  • Minisatellite Repeats

References

This article includes 25 references
  1. Dugat T, Lagrée A-C, Maillard R, Boulouis H-J, Haddad N. Opening the black box of Anaplasma phagocytophilum diversity: current situation and future perspectives.. Front Cell Infect Microbiol 2015;61:1–18.
    pmc: PMC4536383pubmed: 26322277
  2. Adams D, Jajosky R, Ajani U, Kriseman J, Sharp P, Onweh D. Morbidity mortality weekly report summary of notifiable diseases. Centers for Disease Control and Prevention 2014.
  3. Cochez C, Ducoffre G, Vandenvelde C, Luyasu V, Heyman P. Human anaplasmosis in Belgium: A 10-year seroepidemiological study. Ticks Tick-Borne Dis 2011;2:156–9.
    doi: 10.1016/j.ttbdis.2011.06.004pubmed: 21890069google scholar: lookup
  4. Edouard S, Koebel C, Goehringer F, Socolovschi C, Jaulhac B, Raoult D. Emergence of human granulocytic anaplasmosis in France. Ticks Tick-Borne Dis 2012;3:403–5.
    doi: 10.1016/j.ttbdis.2012.10.002pubmed: 23182272google scholar: lookup
  5. Scharf W, Schauer S, Freyburger F, Petrovec M, Schaarschmidt-Kiener D, Liebisch G. Distinct host species correlate with Anaplasma phagocytophilum ankA gene clusters. J Clin Microbiol 2011;49:790–6.
    doi: 10.1128/JCM.02051-10pmc: PMC3067700pubmed: 21177886google scholar: lookup
  6. Dugat T, Chastagner A, Lagrée A-C, Petit E, Durand B, Thierry S. A new multiple-locus variable-number tandem repeat analysis reveals different clusters for Anaplasma phagocytophilum circulating in domestic and wild ruminants. Parasit Vectors 2014;7:439.
    doi: 10.1186/1756-3305-7-439pmc: PMC4262125pubmed: 25228371google scholar: lookup
  7. Chastagner A, Dugat T, Vourc HG, Verheyden H, Legrand L, Bachy V. Multilocus sequence analysis of Anaplasma phagocytophilum reveals three distinct lineages with different host ranges in clinically ill French cattle. Vet Res 2014;45:114.
    doi: 10.1186/s13567-014-0114-7pmc: PMC4334609pubmed: 25487348google scholar: lookup
  8. Huhn C, Winter C, Wolfsperger T, Wüppenhorst N, Strašek Smrdel K, Skuballa J. Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing. PLoS One 2014;9:e93725.
    pmc: PMC3974813pubmed: 24699849
  9. Majazki J, Wüppenhorst N, Hartelt K, Birtles R, von Loewenich FD. Anaplasma phagocytophilum strains from voles and shrews exhibit specific ankA gene sequences. BMC Vet Res 2013;9:235.
    doi: 10.1186/1746-6148-9-235pmc: PMC4220824pubmed: 24283328google scholar: lookup
  10. Silaghi C, Pfister K, Overzier E. Molecular investigation for bacterial and protozoan tick-borne pathogens in wild boars (Sus scrofa) from southern Germany. Vector Borne Zoonotic Dis 2014;14:371–3.
    doi: 10.1089/vbz.2013.1495pmc: PMC4025625pubmed: 24745766google scholar: lookup
  11. Bown KJ, Lambin X, Ogden NH, Begon M, Telford G, Woldehiwet Z. Delineating Anaplasma phagocytophilum ecotypes in coexisting, discrete enzootic cycles. Emerg Infect Dis 2009;15:1948–54.
    doi: 10.3201/eid1512.090178pmc: PMC3044514pubmed: 19961674google scholar: lookup
  12. Blaňarová L, Stanko M, Carpi G, Miklisová D, Víchová B, Mošanský L. Distinct Anaplasma phagocytophilum genotypes associated with Ixodes trianguliceps ticks and rodents in Central Europe. Ticks Tick-Borne Dis 2014;6:928–38.
    doi: 10.1016/j.ttbdis.2014.07.012pubmed: 25129860google scholar: lookup
  13. Courtney JW, Kostelnik LM, Zeidner NS, Massung RF. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol 2004;42:3164–8.
  14. Chen SM, Dumler JS, Bakken JS, Walker DH. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 1994;32:589–95.
    pmc: PMC263091pubmed: 8195363
  15. Dugat T, Haciane D, Durand B, Lagrée A-C, Haddad N, Boulouis H-J. Short report: Identification of a potential marker of Anaplasma phagocytophilum associated with cattle abortion. Transbound Emerg Dis 2016. In press.
    pubmed: 27090504
  16. . R: a language and environment for statistical computing. 2009.
  17. Jahfari S, Coipan EC, Fonville M, van Leeuwen AD, Hengeveld P, Heylen D. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasit Vectors 2014;7:365.
    doi: 10.1186/1756-3305-7-365pmc: PMC4153903pubmed: 25127547google scholar: lookup
  18. Stuen S, Pettersen KS, Granquist EG, Bergström K, Bown KJ, Birtles RJ. Anaplasma phagocytophilumvariants in sympatric red deer (Cervus elaphus) and sheep in southern Norway. Ticks Tick-Borne Dis 2013;4:197–201.
    doi: 10.1016/j.ttbdis.2012.11.014pubmed: 23414797google scholar: lookup
  19. Stuen S, Granquist EG, Silaghi C. Anaplasma phagocytophilum - a widespread multi-host pathogen with highly adaptive strategies. Front Cell Infect Microbiol 2013;3:31.
    doi: 10.3389/fcimb.2013.00031pmc: PMC3717505pubmed: 23885337google scholar: lookup
  20. Nahayo A, Bardiau M, Volpe R, Pirson J, Paternostre J, Fett T. Molecular evidence of Anaplasma phagocytophilum in wild boar (Sus scrofa) in Belgium. BMC Vet Res 2014;10:80.
    doi: 10.1186/1746-6148-10-80pmc: PMC3976503pubmed: 24694049google scholar: lookup
  21. De La Fuente J, Naranjo V, Ruiz-Fons F, Höfle U, Fernández De Mera IG, Villanúa D. Potential vertebrate reservoir hosts and invertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector Borne Zoonotic Dis Larchmt N 2005;5:390–401.
    doi: 10.1089/vbz.2005.5.390pubmed: 16417435google scholar: lookup
  22. Masuzawa T, Uchishima Y, Fukui T, Okamoto Y, Muto M, Koizumi N. Detection of Anaplasma phagocytophilum from wild boars and deer in Japan. Jpn J Infect Dis 2011;64:333–6.
    pubmed: 21788712
  23. Galindo RC, Ayllon N, Smrdel KS, Boadella M, Beltran-Beck B, Mazariegos M. Gene expression profile suggests that pigs (Sus scrofa) are susceptible to Anaplasma phagocytophilum but control infection. Parasit Vectors 2012;5:181.
    doi: 10.1186/1756-3305-5-181pmc: PMC3453518pubmed: 22935149google scholar: lookup
  24. Aardema ML, von Loewenich FD. Varying influences of selection and demography in host-adapted populations of the tick-transmitted bacterium, Anaplasma phagocytophilum. BMC Evol Biol 2015;15:58.
    doi: 10.1186/s12862-015-0335-zpmc: PMC4383208pubmed: 25888490google scholar: lookup
  25. Thomas RJ, Birtles RJ, Radford AD, Woldehiwet Z. Recurrent bacteraemia in sheep infected persistently with Anaplasma phagocytophilum. J Comp Pathol 2012;147:360–7.
    pubmed: 22520814