Rev. Inst. Med. trop. S. Paulo vol.60  São Paulo  2018  Epub Sep 13, 2018

Letter to the Editor

Molecular detection of Borrelia burgdorferi in free-living golden headed lion tamarins (Leontopithecus chrysomelas) in Rio de Janeiro, Brazil

Aline Vieira Pinheiro dos Santos1  Aline Moreira de Souza1  Marina Galvão Bueno2  3  José Luiz Catao-Dias4  Helena Keiko Toma5  Alcides Pissinati4  6  Camila Vieira Molina2  Maria Cecília Martins Kierulff2  7  Danilo Gomes Freitas Silva2  4  Nádia Regina Pereira Almosny1 


Borreliosis is an infectious disease caused by Borrelia spirochetes, transmitted mainly by Ixodes ricinus ticks1 to animals or humans2. The known Borrelia species determine five distinct disease groups: human recurrent fever, avian borreliosis, bovine borreliosis, Lyme borreliosis and bovine scrapie36. Lyme disease (LD) is a multisystem disease with a wide geographical distribution and has B. burgdorferi as the main agent in several continents5,7.

In Brazil, borreliosis is called Brazilian Lyme-like disease, Baggio-Yoshinari Syndrome or Brazilian Borreliosis (BB), is transmitted by ticks that are not from the Ixodes ricinus complex, and is caused by B. burgdorferi sensu lato8.

Borrelia species were described in non-human primates that currently serve as an experimental model for Lyme disease2,911.

Borrelia species are transmitted primarily by ticks, but in rare cases or experimentally, they can be transmitted by tabanids, culicides and siphonapters12. Studies on borreliosis have been carried out to compare immunological, histopathological and clinical responses of animals and humans infected with Borrelia burgdorferi. In these studies, animals were inoculated or exposed to the Ixodides dammini tick1,9,11, and findings such as conjunctivitis, rash, deep perivascular lymphocytic infiltration that are characteristic in humans1, a large amount of spirochetes in nervous tissue of immunosuppressed animals9 and spirochetes in cardiac tissue10 were reported.

In order to identify arthropod-borne pathogens in an exotic invasive population of Leontopithecus chrysomelas (golden-headed lion tamarin), that inhabit Serra da Tiririca State Park (PESET), an urban Atlantic Rainforest area in Niteroi (Rio de Janeiro, Brazil), to translocate them to their native area (Bahia, Brazil), blood samples were analyzed. PESET harbor a large diversity of endemic fauna and flora and is considered an important ecotourism area. Inappropriate housing constructions, the increase of human and animal populations living inside the park or in its surroundings, hunting and inadequate garbage disposal have been recently causing damage to the park13.

This study was approved by the Ethics Commission on Animal Use (CEUA) from Universidade Federal Fluminense (process N° 367, issued in 10/10/2013) and was in full compliance with the federal authorizations issued by the Environment Ministry (SISBIO n 30939-4 issued in 18/05/2012). All procedures were also approved by the Committee on Ethics on Animal Research (CEUA) of Veterinary Medicine and Animal Science Faculty of the Universidade de Sao Paulo (Protocol N° 2662/2012 and 7085041215).

Blood samples of 200 L. chrysomelas, males and females, of different ages and independent of clinical alterations were subjected to DNA extraction using the Illustra blood genomic Prep Mini Spin Kit (GE Healthcare Life Sciences, Sao Paulo, Brazil), according to the manufacturer instructions. Extracted DNA was then used as the template DNA in B. burgdorferi sensu lato (s.l.) amplifications. Nested Polymerase Chain Reaction (n-PCR) assay using primer 5Bor-out (5′-GTCAAACGGGATGTAGCAA TAC-3′) and 3Bor-out (5′-CACACTTAACACGTTAGCTTCG-3′), followed by a second reaction with primer 5Bor-in (5′-ATTCAGTGGCGAACGGGTG-3′) and 3Bor-in (5′-AACAACGCTCGCCCCTTAC-3′), which amplifies a fragment of 811 bp/ 469 bp of the 16S rRNA gene of B. burgdorferi sensu lato, were performed.

A total of 16% (32/200) L. chrysomelas were positive to B. burgdorferi by n-PCR. Sequencing of five positive samples showed 99% of similarity with B. burgdorferi sequences available in GenBank. This was the first time that borreliosis is found in non- human primates in Brazil.

Borrelia infection in humans was first described in Brazil in 1992, and has an increasing number of suspect cases, differing from LD due to the recurrence rate after treatment and the intense immune response8. The presence of Borrelia burgdorferi in free-living golden-headed lion tamarins that inhabit Atlantic Forest biome of Rio de Janeiro, Brazil, confirms that this spirochete is circulating in this region and suggests that these small primates may play a role in transmission of this pathogen to other animals or human beings. Veterinarians and medical doctors should consider this zoonotic pathogen in their diagnostic routine.

Further studies are needed, including sequencing of all positive samples, in order to compare these small primates positive sequences with those of humans and other animals in study area.


1. Philipp MT, Aydintug MK, Bohm RP Jr, Cogswell FB, Dennis VA, Lanners HN, et al. Early and early disseminated phases of Lyme disease in the rhesus monkey: a model for infection in humans. Infect Immun. 1993;61:3047-59. [ Links ]

2. Soares CO, Ishikawa MM, Fonseca AH, Yoshinari NH. Borrelioses, agentes e vetores. Pesq Vet Bras. 2000;20:1-19. [ Links ]

3. Babour AG, Hayes SF. Biology of Borrelia species. Microbiol Rev. 1986;50:381-400. [ Links ]

4. Quinn PJ, Carter ME, Markey BK, Carter GR. Clinical veterinary microbiology. London: Wolfe; 1994. [ Links ]

5. Wang G, van Dam AP, Le Fleche A, Postic D, Peter O, Baranton G, et al. Genetic and phenotypic analysis of Borrelia valaisiana sp. nov. (Borrelia genomic groups VS116 and M19). Int J Syst Bacteriol. 1997;47:926-32. [ Links ]

6. Zingg BC, LeFebvre RB. Polymerase chain reaction for detection of Borrelia coriaceae, putative agent of epizootic bovine abortion. Am J Vet Res. 1994;55:1509-15. [ Links ]

7. Bennett CE. Ticks and Lyme diseases. Adv Parasitol. 1995;36:343-405. [ Links ]

8. Basile RC, Yoshinari NH, Mantovani E, Bonoldi VN, Macoris DG, Queiroz-Neto A. Brazilian borreliosis with special emphasis on humans and horses. Braz J Microbiol. 2017;48:167-72. [ Links ]

9. Cadavid D, O’Neill T, Schaefer H, Pachner R. Localization of Borrelia burgdorferi in the nervous system and other organs in a nonhuman primate model of Lyme disease. Lab Invest. 2000;80:1043-54. [ Links ]

10. Cadavid D, Bai Y, Hodzic E, Narayan K, Barthold SW, Pachner AR. Cardiac involvement in non-human primates infected with the Lyme disease spirochete Borrelia burgdorferi. Lab Invest. 2004;84:1439-50. [ Links ]

11. Roberts ED, Bohm RP Jr, Lowrie RC, Habicht G, Katona L, Piesman J, et al. Pathogenesis of Lyme neuroborreliosis in the rhesus monkey: the early disseminated and chronic phases of disease in the peripheral nervous system. J Infect Dis. 1998;178:722-32. [ Links ]

12. Alvim NC, Bento MA, Martins LA. Borreliose de Lyme: a doença da década. Rev Cient Eletr Med Vet. 2005;4. [ Links ]

13. Instituto Estadual do Ambiente. Resumo executivo: plano de manejo: Parque Estadual da Serra da Tiririca – PESET. Rio de Janeiro: INEA; 2012. [ Links ]

Received: August 13, 2018; Accepted: August 16, 2018


%d bloggers like this: