Infection Kinetics and Tropism of Borrelia burgdorferi sensu lato in Mouse After Natural (via Ticks) or Artificial (Needle) Infection Depends on the Bacterial Strain.

Natacha Sertour,Martine Garnier,Laurence Malandrin,Elisabeth Ferquel,Violaine Cotté,Valérie Choumet

doi:10.3389/fmicb.2018.01722

Natacha Sertour, Martine Garnier + Show 4 more

Open Access

https://doi.org/10.3389/fmicb.2018.01722

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Abstract

Borrelia burgdorferi sl is a complex of pathogen bacteria transmitted to the host by Ixodes ticks. European Ixodes ricinus ticks transmit different B. burgdorferi species, pathogenic to human. Bacteria are principally present in unfed tick midgut, then migrate to salivary glands during blood meal and infect a new host via saliva. In this study, efficiency of transmission in a mouse model of three pathogen species belonging to the B. burgdorferi sl complex, B. burgdorferi sensu stricto (B31, N40, and BRE-13), B. afzelii (IBS-5), and B. bavariensis (PBi) is examined in order to evaluate infection risk after tick bite. We compared the dissemination of the Borrelia species in mice after tick bite and needle injection. Location in the ticks and transmission to mice were also determined for the three species by following infection kinetics. After inoculation, we found a significant prevalence in the brain for PBi and BRE-13, in the heart, for PBi, in the skin where B31 was more prevalent than PBi and in the ankle where both B31 and N40 were more present than PBi. After tick bite, statistical analyses showed that BRE-13 was more prevalent than N40 in the brain, in the bladder and in the inguinal lymph node. When Borrelia dissemination was compared after inoculation and tick bite, we observed heart infection only after tick inoculation of BRE-13, and PBi was only detected after tick bite in the skin. For N40, a higher number of positive organs was found after inoculation compared to tick bite. All European B. burgdorferi sl strains studied were detected in female salivary glands before blood meal and infected mice within 24 h of tick bite. Moreover, Borrelia-infected nymphs were able to infect mice as early as 12 h of tick attachment. Our study shows the need to remove ticks as early as possible after attachment. Moreover, Borrelia tropism varied according to the strain as well as between ticks bite and needle inoculation, confirming the association between some strains and clinical manifestation of Lyme borreliosis, as well as the role played by tick saliva in the efficiency of Borrelia infection and dissemination in vertebrates.

Highlights

Lyme borreliosis (LB) is the most commonly occurring vectorborne disease in Europe
For B. burgdorferi ss BRE-13 strain, Borrelia DNA was detected in ear biopsies from 20% of mice after 14 days and 70% of mice after 21 days. 90% of mice were found positive by specific DNA amplification 14 days after inoculation of the B. burgdorferi ss N40 strain
DNA B. burgdorferi sl was detected in the ears of mice infected with B. bavariensis PBi strain after 3 weeks in 60% of them and in 80% of mice after 28 days

Summary

Introduction

Lyme borreliosis (LB) is the most commonly occurring vectorborne disease in Europe. It is caused by spirochetes belonging to the Borrelia burgdorferi sensu lato (sl) complex. This complex comprises species: Borrelia burgdorferi sensu stricto (ss), B. afzelii, B. garinii, B. bavariensis, B. spielmanii, B. valaisiana and B. lusitaniae (Rijpkema et al, 1997; Collares-Pereira et al, 2004; Rudenko et al, 2011; Stanek et al, 2011). The bacteria are transmitted by a hard tick bite of Ixodes genus. Ticks can parasitize a wide range of hosts. Some of them may be reservoirs for Borrelia, humans being considered as accidental hosts

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