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Volume 25, Number 7—July 2019
Research Letter

Zoonotic Bacteria in Fleas Parasitizing Common Voles, Northwestern Spain

Ruth Rodríguez-Pastor1Comments to Author , François Mougeot, Mª Dolors Vidal, Isabel Jado, Rosa M. González-Martín-Niño, Raquel Escudero2, and Juan José Luque-Larena2
Author affiliations: Universidad de Valladolid and Instituto Universitario de Investigación en Gestión Forestal Sostenible, Palencia, Spain (R. Rodríguez-Pastor, J.J. Luque-Larena); Instituto de Investigación en Recursos Cinegéticos, Ciudad Real, Spain (F. Mougeot); Universidad de Castilla-La Mancha, Ciudad Real (M.D. Vidal); Instituto de Salud Carlos III, Madrid, Spain (I. Jado, R.M. González-Martín-Niño, R. Escudero)

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Abstract

We detected Francisella tularensis and Bartonella spp. in fleas parasitizing common voles (Microtus arvalis) from northwestern Spain; mean prevalence was 6.1% for F. tularensis and 51% for Bartonella spp. Contrasted vector–host associations in the prevalence of these bacteria suggest that fleas have distinct roles in the transmission cycle of each pathogen in nature.

A dynamic prevalence of Francisella tularensis and Bartonella spp. was reported in irruptive common vole (Microtus arvalis) populations during 2013–2015 from agricultural landscapes of northwestern Spain (1,2). In that area, notifiable tularemia has been endemic since 1997, and human cases periodically occur during outbreaks in voles (3,4). Prevalence of F. tularensis and Bartonella spp. in voles increases with vole density (1,2), highlighting the key role of fluctuating rodents in shaping zoonoses dynamics (14). Rodent ectoparasites often play a major role in transmitting zoonotic pathogens. In the population studied, ticks rarely infest voles (2% prevalence), whereas fleas are much more prevalent (68%) (2). Nevertheless, any potential role for vole fleas in the circulation of F. tularensis or Bartonella spp. in natural environments remains unknown. To elucidate realistic transmission route scenarios in host-dynamic environments (58), we investigated whether zoonotic bacteria occur concomitantly in voles and fleas.

Our main goal was to study the prevalence of F. tularensis in fleas collected from voles previously tested for tularemia (1). We screened flea DNA in search of 6 main zoonotic bacteria simultaneously (Anaplasma phagocytophilum, Bartonella spp., Borrelia spp., Coxiella burnetii, F. tularensis, and Rickettsia spp.), following the same molecular procedure (multiplex PCR) (9) previously used to screen vole pathogens (1,2). Voles and fleas were live-trapped in northwestern Spain during March 2013–March 2015 (Appendix). We collected fleas from each individual vole and identified and grouped them in pools (pool = total fleas/vole). Three flea species parasitize common voles in the area: Ctenophthalmus apertus, Nosopsyllus fasciatus, and Leptopsylla taschenbergi (2). We screened monospecific pools (all fleas in a pool belonged to the same species and came from the same vole host), for a sample size of 90 vole hosts (pools) and 191 fleas. We screened 78 C. apertus fleas (39 pools) and 113 N. fasciatus fleas (51 pools). Among the 90 voles providing fleas, 27 were F. tularensis PCR–positive; the remaining 63 were negative (1). Of these same 90 voles, 45 were Bartonella PCR–positive and 45 were negative. Seventeen were positive for both F. tularensis and Bartonella spp. (2).

Flea pools had an average of 2.12 fleas (range 1–9); however, most (>70%) contained 1 (51%) or 2 (22%) fleas (Table). We did not detect DNA from pathogens other than F. tularensis and Bartonella spp. in fleas. Three (3%) flea pools harbored F. tularensis DNA; we estimated the overall prevalence at 6%. F. tularensis prevalence in both flea species was low (1 positive pool of 51 in N. fasciatus and 2 of 39 in C. apertus). All F. tularensis PCR–positive flea pools came from F. tularensis PCR–positive voles, and prevalence of F. tularensis in fleas was significantly associated with its prevalence in voles (analysis of variance [ANOVA], R2 = 0.072, F0.05, 1, 88 = 6.81; p = 0.011). Of note, all fleas containing F. tularensis DNA were collected during July 2014, when vole populations reached top densities and tularemia prevalence peaked among them (33%) (1). The low prevalence of F. tularensis detected in fleas carried by infected hosts (3 of 27 pools) and the detection of infected flea pools only when abundance of the bacterium in the environment was highest (during vole peaks) (1,4) suggest that the quantitative role of fleas in the circulation of F. tularensis might be modest.

Conversely, the role of fleas in the circulation of Bartonella spp. seems much more relevant. We detected Bartonella spp. in 28 (37%) flea pools and in both flea species (37% of N. fasciatus and 23% of C. apertus) (Table). We detected Bartonella spp. in fleas collected from Bartonella PCR–positive and Bartonella PCR–negative voles in nearly equal proportions (51% vs. 44%) (Table). The average prevalence of Bartonella spp. in fleas was not associated with its prevalence in voles (ANOVA, R2 = 0.006, F0.05, 1, 88 = 0.53; p = 0.467). We found a higher Bartonella spp. prevalence in N. fasciatus (65%) than in C. apertus (33%). We identified 3 Bartonella species among fleas (B. taylorii [17%], B. grahamii [14%], and B. rochalimae [3%]), as well as mixed infections (Appendix). These findings are in accordance with other research showing fleas as a main vector of Bartonella spp. (5). Although F. tularensis and Bartonella spp. have been simultaneously detected in ≈13% of voles during population density peaks (2), we identified no co-infection among flea pools (ANOVA, R2 = 0.011, F0.05, 1, 88 = 0.97; p = 0.328).

Our data show that F. tularensis and Bartonella spp. occur in the fleas infesting wild common voles in northwestern Spain, with notable differences in prevalence (6% and 51%, respectively) and associations with prevalence in vole hosts. Future studies are needed to determine the role of fleas in the circulation of these pathogens in nature and in particular to ascertain any effective vectoring of F. tularensis.

Dr. Rodríguez-Pastor is a postdoctoral student at the Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel. Her research interests include the ecology of zoonoses and disease dynamics in animal populations, specifically parasite and infectious pathogen dynamics in wild rodents.

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Acknowledgments

We thank Fabio Flechoso for helping with ectoparasite counts and flea identification.

This work was supported by ECOVOLE (Factores ecológicos que influyen en la reproducción y dinámica poblacional del topillo campesino (Microtus arvalis) en medios agrarios; CGL2012-35348), ECOTULA (Ecología de la Tularemia: dinámica espacio-temporal, ciclos ecológicos de transmisión y mapas de riesgo en ecosistemas agrarios del NO de España; CGL2015-66962-C2-1-R), and RESERTULA (Microbiología de la Tularemia: circulación de Francisella tularensis en los ecosistemas agrarios del NO de España. Estudio d relaciones epidemiológicas y filogenéticas; CLG2015-66962-C2-2-R) projects funded by the Government of Spain (lMINECO/FEDER). R.R.-P. was supported by a PhD studentship from the University of Valladolid (co-funded by Banco Santander, RR 30/04/2014).

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References

  1. Rodríguez-Pastor  R, Escudero  R, Vidal  D, Mougeot  F, Arroyo  B, Lambin  X, et al. Density-dependent prevalence of Francisella tularensis in fluctuating vole populations, northwestern Spain. Emerg Infect Dis. 2017;23:13779. DOIPubMed
  2. Rodríguez-Pastor  R, Escudero  R, Lambin  X, Vidal  MD, Gil  H, Jado  I, et al. Zoonotic pathogens in fluctuating common vole (Microtus arvalis) populations: occurrence and dynamics. Parasitology. 2019;146:38998. DOIPubMed
  3. Luque-Larena  JJ, Mougeot  F, Roig  DV, Lambin  X, Rodríguez-Pastor  R, Rodríguez-Valín  E, et al. Tularemia outbreaks and common vole (Microtus arvalis) irruptive population dynamics in northwestern Spain, 1997–2014. Vector Borne Zoonotic Dis. 2015;15:56870. DOIPubMed
  4. Luque-Larena  JJ, Mougeot  F, Arroyo  B, Vidal  MD, Rodríguez-Pastor  R, Escudero  R, et al. Irruptive mammal host populations shape tularemia epidemiology. PLoS Pathog. 2017;13:e1006622. DOIPubMed
  5. Gutiérrez  R, Krasnov  B, Morick  D, Gottlieb  Y, Khokhlova  IS, Harrus  S. Bartonella infection in rodents and their flea ectoparasites: an overview. Vector Borne Zoonotic Dis. 2015;15:2739. DOIPubMed
  6. Silaghi  C, Pfeffer  M, Kiefer  D, Kiefer  M, Obiegala  A. Bartonella, rodents, fleas and ticks: a molecular field study on host–vector-pathogen associations in Saxony, eastern Germany. Microb Ecol. 2016;72:96574. DOIPubMed
  7. Hornok  S, Földvári  G, Rigó  K, Meli  ML, Gönczi  E, Répási  A, et al. Synanthropic rodents and their ectoparasites as carriers of a novel haemoplasma and vector-borne, zoonotic pathogens indoors. Parasit Vectors. 2015;8:27. DOIPubMed
  8. Stevenson  HL, Bai  Y, Kosoy  MY, Montenieri  JA, Lowell  JL, Chu  MC, et al. Detection of novel Bartonella strains and Yersinia pestis in prairie dogs and their fleas (Siphonaptera: Ceratophyllidae and Pulicidae) using multiplex polymerase chain reaction. J Med Entomol. 2003;40:32937. DOIPubMed
  9. Anda  P, Escudero  R, Rodriguez-Moreno  I, Jado  I, Jimenez-Alonso  MI. Method and kit for the detection of bacterial species by means of DNA analysis. European patent EP1895015B1. 2012 July 25.

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Table

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Cite This Article

DOI: 10.3201/eid2507.181646

Original Publication Date: 6/10/2019

1Current affiliation: Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel.

2These authors contributed equally to this article.

Table of Contents – Volume 25, Number 7—July 2019

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Ruth Rodríguez-Pastor, Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, 84990, Israel

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Page created: June 17, 2019
Page updated: June 17, 2019
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