Rapid clearance of Borrelia burgdorferi from the blood circulation

Abstract Background Borrelia burgdorferi is a tick-borne spirochete that causes Lyme borreliosis (LB). After an initial tick bite, it spreads from the deposition site in the dermis to distant tissues of the host. It is generally believed that this spirochete disseminates via the hematogenous route....

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Main Authors: Liucun Liang, Jinyong Wang, Lucas Schorter, Thu Phong Nguyen Trong, Shari Fell, Sebastian Ulrich, Reinhard K. Straubinger
Format: Article
Language:English
Published: BMC 2020-04-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-020-04060-y
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author Liucun Liang
Jinyong Wang
Lucas Schorter
Thu Phong Nguyen Trong
Shari Fell
Sebastian Ulrich
Reinhard K. Straubinger
author_facet Liucun Liang
Jinyong Wang
Lucas Schorter
Thu Phong Nguyen Trong
Shari Fell
Sebastian Ulrich
Reinhard K. Straubinger
author_sort Liucun Liang
collection DOAJ
description Abstract Background Borrelia burgdorferi is a tick-borne spirochete that causes Lyme borreliosis (LB). After an initial tick bite, it spreads from the deposition site in the dermis to distant tissues of the host. It is generally believed that this spirochete disseminates via the hematogenous route. Borrelia persica causes relapsing fever and is able to replicate in the blood stream. Currently the exact dissemination pathway of LB pathogens in the host is not known and controversially discussed. Methods In this study, we established a strict intravenous infection murine model using host-adapted spirochetes. Survival capacity and infectivity of host-adapted B. burgdorferi sensu stricto (Bbss) were compared to those of B. persica (Bp) after either intradermal (ID) injection into the dorsal skin of immunocompetent mice or strict intravenous (IV) inoculation via the jugular vein. By in vitro culture and PCR, viable spirochetes and their DNA load in peripheral blood were periodically monitored during a 49/50-day course post-injection, as well as in various tissue samples collected at day 49/50. Specific antibodies in individual plasma/serum samples were detected with serological methods. Results Regardless of ID or IV injection, DNA of Bp was present in blood samples up to day 24 post-challenge, while no Bbss was detectable in the blood circulation during the complete observation period. In contrast to the brain tropism of Bp, Bbss spirochetes were found in ear, skin, joint, bladder, and heart tissue samples of only ID-inoculated mice. All tested tissues collected from IV-challenged mice were negative for traces of Bbss. ELISA testing of serum samples showed that Bp induced gradually increasing antibody levels after ID or IV inoculation, while Bbss did so only after ID injection but not after IV inoculation. Conclusions This study allows us to draw the following conclusions: (i) Bp survives in the blood and disseminates to the host’s brain via the hematogenous route; and (ii) Bbss, in contrast, is cleared rapidly from the blood stream and is a tissue-bound spirochete.
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spelling doaj.art-d127d0d6193b40d69a12d3a77dc923b32022-12-22T00:16:19ZengBMCParasites & Vectors1756-33052020-04-0113111710.1186/s13071-020-04060-yRapid clearance of Borrelia burgdorferi from the blood circulationLiucun Liang0Jinyong Wang1Lucas Schorter2Thu Phong Nguyen Trong3Shari Fell4Sebastian Ulrich5Reinhard K. Straubinger6Bacteriology and Mycology, Institute for Infectious Diseases and Zoonoses, Department of Veterinary Science, Faculty of Veterinary Medicine, LMU MunichDepartment of Microbiology & Immunology, Chicago Medical School, Rosalind Franklin University of Medicine and ScienceBacteriology and Mycology, Institute for Infectious Diseases and Zoonoses, Department of Veterinary Science, Faculty of Veterinary Medicine, LMU MunichBacteriology and Mycology, Institute for Infectious Diseases and Zoonoses, Department of Veterinary Science, Faculty of Veterinary Medicine, LMU MunichBacteriology and Mycology, Institute for Infectious Diseases and Zoonoses, Department of Veterinary Science, Faculty of Veterinary Medicine, LMU MunichBacteriology and Mycology, Institute for Infectious Diseases and Zoonoses, Department of Veterinary Science, Faculty of Veterinary Medicine, LMU MunichBacteriology and Mycology, Institute for Infectious Diseases and Zoonoses, Department of Veterinary Science, Faculty of Veterinary Medicine, LMU MunichAbstract Background Borrelia burgdorferi is a tick-borne spirochete that causes Lyme borreliosis (LB). After an initial tick bite, it spreads from the deposition site in the dermis to distant tissues of the host. It is generally believed that this spirochete disseminates via the hematogenous route. Borrelia persica causes relapsing fever and is able to replicate in the blood stream. Currently the exact dissemination pathway of LB pathogens in the host is not known and controversially discussed. Methods In this study, we established a strict intravenous infection murine model using host-adapted spirochetes. Survival capacity and infectivity of host-adapted B. burgdorferi sensu stricto (Bbss) were compared to those of B. persica (Bp) after either intradermal (ID) injection into the dorsal skin of immunocompetent mice or strict intravenous (IV) inoculation via the jugular vein. By in vitro culture and PCR, viable spirochetes and their DNA load in peripheral blood were periodically monitored during a 49/50-day course post-injection, as well as in various tissue samples collected at day 49/50. Specific antibodies in individual plasma/serum samples were detected with serological methods. Results Regardless of ID or IV injection, DNA of Bp was present in blood samples up to day 24 post-challenge, while no Bbss was detectable in the blood circulation during the complete observation period. In contrast to the brain tropism of Bp, Bbss spirochetes were found in ear, skin, joint, bladder, and heart tissue samples of only ID-inoculated mice. All tested tissues collected from IV-challenged mice were negative for traces of Bbss. ELISA testing of serum samples showed that Bp induced gradually increasing antibody levels after ID or IV inoculation, while Bbss did so only after ID injection but not after IV inoculation. Conclusions This study allows us to draw the following conclusions: (i) Bp survives in the blood and disseminates to the host’s brain via the hematogenous route; and (ii) Bbss, in contrast, is cleared rapidly from the blood stream and is a tissue-bound spirochete.http://link.springer.com/article/10.1186/s13071-020-04060-yLyme borreliosisBorrelia burgdorferiTick-borne relapsing feverBorrelia persicaBlood clearance
spellingShingle Liucun Liang
Jinyong Wang
Lucas Schorter
Thu Phong Nguyen Trong
Shari Fell
Sebastian Ulrich
Reinhard K. Straubinger
Rapid clearance of Borrelia burgdorferi from the blood circulation
Parasites & Vectors
Lyme borreliosis
Borrelia burgdorferi
Tick-borne relapsing fever
Borrelia persica
Blood clearance
title Rapid clearance of Borrelia burgdorferi from the blood circulation
title_full Rapid clearance of Borrelia burgdorferi from the blood circulation
title_fullStr Rapid clearance of Borrelia burgdorferi from the blood circulation
title_full_unstemmed Rapid clearance of Borrelia burgdorferi from the blood circulation
title_short Rapid clearance of Borrelia burgdorferi from the blood circulation
title_sort rapid clearance of borrelia burgdorferi from the blood circulation
topic Lyme borreliosis
Borrelia burgdorferi
Tick-borne relapsing fever
Borrelia persica
Blood clearance
url http://link.springer.com/article/10.1186/s13071-020-04060-y
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