Ecoepidemiological determinants of Borrelia infection in sigmodontine rodents from the Delta and Parana Islands ecoregion, Argentina

1. White, R. J. & Razgour, O. Emerging zoonotic diseases originating in mammals: A systematic review of effects of anthropogenic land‐use change. Mammal Rev. 50, 336–352 (2020).

   Google Scholar 

2. Jones, B. A. et al. Zoonosis emergence linked to agricultural intensification and environmental change. Proc. Natl. Acad. Sci. U. S. A. 110, 8399–8404 (2013).

   Google Scholar 

3. Morens, D. M., Folkers, G. K. & Fauci, A. S. The challenge of emerging and re-emerging infectious diseases. Nature 430, 242–249 (2004).

   Google Scholar 

4. Jongejan, F. & Uilenberg, G. The global importance of ticks. Parasitology 129, S3–S14 (2004).

   Google Scholar 

5. de la Fuente, J. Overview: Ticks as vectors of pathogens that cause disease in humans and animals.. Front. Biosci. https://doi.org/10.2741/3200 (2008).

   Google Scholar 

6. Brouqui, P. & Matsumoto, K. Bacteriology and phylogeny of Anaplasmataceae. In Rickettsial Diseases (eds Raoult, D. & Parola, P.) 179–198 (Informa Healthcare, 2007). https://doi.org/10.3109/9781420019971.013.

   Google Scholar 

7. Rollend, L., Fish, D. & Childs, J. E. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: A summary of the literature and recent observations. Ticks. Tick. Borne. Dis. 4, 46–51 (2013).

   Google Scholar 

8. Gervasi, S. S., Civitello, D. J., Kilvitis, H. J. & Martin, L. B. The context of host competence: A role for plasticity in host–parasite dynamics. Trends Parasitol. 31, 419–425 (2015).

   Google Scholar 

9. Ostfeld, R. S., Levi, T., Keesing, F., Oggenfuss, K. & Canham, C. D. Tick‐borne disease risk in a forest food web. Ecology 99, 1562–1573 (2018).

   Google Scholar 

10. Rudenko, N., Golovchenko, M., Grubhoffer, L. & Oliver, J. H. Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks. Tick. Borne. Dis. 2, 123–128 (2011).

    Google Scholar 

11. Marques, A. R., Strle, F. & Wormser, G. P. Comparison of Lyme disease in the United States and Europe. Emerg. Infect. Dis. 27, 2017–2024 (2021).

    Google Scholar 

12. Krawczyk, A. I. et al. Effect of rodent density on tick and tick-borne pathogen populations: Consequences for infectious disease risk. Parasit. Vectors. 13, 34 (2020).

    Google Scholar 

13. Wolcott, K. A., Margos, G., Fingerle, V. & Becker, N. S. Host association of Borrelia burgdorferi sensu lato: A review. Ticks Tick-Borne Dis. 12, 101766 (2021).

    Google Scholar 

14. Barolin, J., Antoniazzi, L. R., Colombo, V. C., Beldomenico, P. M. & Monje, L. D. Sigmodontinae rodents as potential reservoirs for Borrelia burgdorferi sensu lato in the Delta and Paraná Islands ecoregion, Argentina.. Med. Vet. Entomol. https://doi.org/10.1111/mve.12766 (2024).

    Google Scholar 

15. Mancilla-Agrono, L. Y. et al. Is Borrelia burgdorferi sensu stricto in South America? First molecular evidence of its presence in Colombia. Trop. Med. Infect. Dis. 7, 428 (2022).

    Google Scholar 

16. Sánchez, R. S. T. et al. Rodents as potential reservoirs for Borrelia spp. in northern Chile.. Rev. Bras. Parasitol. Vet. 29, e000120 (2020).

    Google Scholar 

17. Weck, B. C., Serpa, M. C. A., Labruna, M. B. & Muñoz-Leal, S. A Novel Genospecies of Borrelia burgdorferi sensu lato associated with cricetid rodents in Brazil. Microorganisms 10, 204 (2022).

    Google Scholar 

18. Cicuttin, G. L., De Salvo, M. N., Venzal, J. M. & Nava, S. Borrelia spp. in ticks and birds from a protected urban area in Buenos Aires city, Argentina.. Ticks Tick Borne Dis. 10, 101282 (2019).

    Google Scholar 

19. Flores, F. S., Muñoz-Leal, S., Diaz, A. & Labruna, M. B. Wild birds as host of Borrelia burgdorferi sensu lato in northwestern Argentina. Ticks Tick-Borne Dis. 9, 1586–1589 (2018).

    Google Scholar 

20. Nava, S. et al. Borrelia infection in Ixodes pararicinus ticks (Acari: Ixodidae) from northwestern Argentina. Acta Trop. 139, 1–4 (2014).

    Google Scholar 

21. Saracho Bottero, M. N. et al. Presence of Borrelia in different populations of Ixodes pararicinus from northwestern Argentina.. Ticks Tick Borne Dis. 8, 488–493 (2017).

    Google Scholar 

22. Sebastian, P. S. et al. Borrelia burgdorferi sensu lato in Ixodes cf. neuquenensis and Ixodes sigelos ticks from the Patagonian region of Argentina.. Acta Trop. 162, 218–221 (2016).

    Google Scholar 

23. Armitano, R. I. et al. Enfermedad de Lyme. Análisis crítico sobre su presencia en Argentina. Medicina (Mex.) (2024).

24. Labruna, M. B., Faccini-Martínez, Á. A., Muñoz-Leal, S., Szabó, M. P. J. & Angerami, R. N. Lyme borreliosis in Brazil: A critical review on the Baggio–Yoshinari syndrome (Brazilian Lyme-like disease).. Clin. Microbiol. Rev. https://doi.org/10.1128/cmr.00097-24 (2024).

    Google Scholar 

25. Miziara, C. S. M. G., Gelmeti Serrano, V. A. & Yoshinari, N. Passage of Borrelia burgdorferi through diverse Ixodid hard ticks causes distinct diseases: Lyme borreliosis and Baggio-Yoshinari syndrome. Clinics 73, e394 (2018).

    Google Scholar 

26. Stanchi, N. O. et al. Retrospective analysis of potential Lyme disease clinical cases in Argentina. Microorganisms 12, 1374 (2024).

    Google Scholar 

27. Goñi, U. “Everything is burning”: Argentina’s delta fires rage out of control. The Guardian (2020).

28. Valente, M. Up in smoke? Argentina’s delta blaze sparks worry – and legal action. Reuters (2020).

29. Kandus, P. & Malvárez, A. I. Vegetation patterns and change analysis in the lower delta islands of the Parana River (Argentina). Wetlands 24, 620–632 (2004).

    Google Scholar 

30. Zoffoli, M. L., Kandus, P., Madanes, N. & Calvo, D. H. Seasonal and interannual analysis of wetlands in South America using NOAA-AVHRR NDVI time series: The case of the Parana Delta Region. Landsc. Ecol. 23, 833–848 (2008).

    Google Scholar 

31. Colombo, V. C. et al. Cattle farming and plantation forest are associated with Bartonella occurrence in wild rodents. EcoHealth 20, 381–389 (2023).

    Google Scholar 

32. Maroli, M., Vadell, M. V., Iglesias, A., Julieta Padula, P. & Gómez Villafañe, I. E. Daily movements and microhabitat selection of Hantavirus reservoirs and other Sigmodontinae rodent species that inhabit a protected natural area of Argentina. EcoHealth 12, 421–431 (2015).

    Google Scholar 

33. Suárez, O. V. & Bonaventura, S. M. Habitat use and diet in sympatric species of rodents of the low Paraná delta, Argentina. Mamm 65, 167–176 (2001).

    Google Scholar 

34. Priotto, J., Steinmann, A. & Polop, J. Factors affecting home range size and overlap in Calomys venustus (Muridae: Sigmodontinae) in Argentine agroecosystems. Mamm. Biol. 67, 97–104 (2002).

    Google Scholar 

35. Steinmann, A. R., Priotto, J. W., Castillo, E. A. & Polop, J. J. Size and overlap of home range in Calomys musculinus (Muridae: Sigmodontinae). Acta Theriol. (Warsz.) 50, 197–206 (2005).

    Google Scholar 

36. Estrada-Peña, A., Venzal, J. M., Mangold, A. J., Cafrune, M. M. & Guglielmone, A. A. The Amblyomma maculatum Koch, 1844 (Acari: Ixodidae: Amblyomminae) tick group: Diagnostic characters, description of the larva of A. parvitarsum Neumann, 1901, 16S rDNA sequences, distribution and hosts. Syst. Parasitol. 60, 99–112 (2005).

    Google Scholar 

37. Martins, T. F., Onofrio, V. C., Barros-Battesti, D. M. & Labruna, M. B. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: Descriptions, redescriptions, and identification key. Ticks Tick-Borne Dis. 1, 75–99 (2010).

    Google Scholar 

38. Marques, S. et al. Redescription of larva, nymph and adults of Ixodes (I.) loricatus Neumann, 1899 (Acari: Ixodidae) based on light and scanning electron microscopy. Syst. Parasitol. 59, 135–146 (2004).

    Google Scholar 

39. Eberhardt, A. T., Monje, L. D., Zurvera, D. A. & Beldomenico, P. M. Detection of Trypanosoma evansi infection in wild capybaras from Argentina using smear microscopy and real-time PCR assays. Vet. Parasitol. 202, 226–233 (2014).

    Google Scholar 

40. Barbour, A. G., Maupin, G. O., Teltow, G. J., Carter, C. J. & Piesman, J. Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: Possible agent of a Lyme disease-like illness. J. Infect. Dis. 173, 403–409 (1996).

    Google Scholar 

41. Bunikis, J. et al. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 150, 1741–1755 (2004).

    Google Scholar 

42. Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

    Google Scholar 

43. Burnham, K. P., Anderson, D. R. & Huyvaert, K. P. AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65, 23–35 (2011).

    Google Scholar 

44. Brisson, D. & Dykhuizen, D. E. ospC Diversity in Borrelia burgdorferi. Genetics 168, 713–722 (2004).

    Google Scholar 

45. Shifflett, S. A. et al. Diversity and host specificity of Borrelia burgdorferi ’s outer surface protein C (ospC) alleles in synanthropic mammals, with a notable ospC allele U absence from mixed infections. Infect. Immun. 92, e00244-e323 (2024).

    Google Scholar 

46. Brunner, J. L. & Ostfeld, R. S. Multiple causes of variable tick burdens on small-mammal hosts. Ecology 89, 2259–2272 (2008).

    Google Scholar 

47. Colombo, V. C. et al. Ecology of the interaction between Ixodes loricatus (Acari: Ixodidae) and Akodon azarae (Rodentia: Criceridae). Parasitol. Res. 114, 3683–3691 (2015).

    Google Scholar 

48. Hofmeister, E. K., Ellis, B. A., Glass, G. E. & Childs, J. E. Longitudinal study of infection with Borrelia burgdorferi in a population of Peromyscus leucopus at a Lyme disease-enzootic site in Maryland. Am. J. Trop. Med. Hyg. 60, 598–609 (1999).

    Google Scholar 

49. Voordouw, M. J., Lachish, S. & Dolan, M. C. The Lyme disease pathogen has no effect on the survival of its rodent reservoir host. PLoS ONE 10, e0118265 (2015).

    Google Scholar 

50. Ginsberg, H. S. et al. Local abundance of Ixodes scapularis in forests: Effects of environmental moisture, vegetation characteristics, and host abundance. Ticks Tick Borne Dis. 11, 101271 (2020).

    Google Scholar 

51. Monje, L. D. et al. Dynamics of exposure to Rickettsia parkeri in cattle in the Paraná River Delta, Argentina. J. Med. Entomol. 53, 660–665 (2016).

    Google Scholar 

52. Aminikhah, M. et al. Rodent host population dynamics drive zoonotic Lyme Borreliosis and Orthohantavirus infections in humans in Northern Europe. Sci. Rep. 11, 16128 (2021).

    Google Scholar 

53. Colombo, V. C. et al. Ecological factors shaping the ectoparasite community assembly of the Azara’s Grass Mouse, Akodon azarae (Rodentia: Cricetidae). Parasitol. Res. 122, 2011–2021 (2023).

    Google Scholar 

54. Nava, S., Venzal, J. M., Martins, T. F., Guglielmone, A. A. & González Acuña, D. Ticks of the Southern Cone of America: Diagnosis, Distribution and Hosts with Taxonomy, Ecology and Sanitary Importance (Academic Press, an impint of Elsevier, 2017).

    Google Scholar 

55. Colombo, V. C. et al. Factors affecting patterns of Amblyomma triste (Acari: Ixodidae) parasitism in a rodent host. Vet. Parasitol. 211, 251–258 (2015).

    Google Scholar 

Download references