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      Transplacental transmission of tick-borne Babesia microti in its natural host Peromyscus leucopus

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          Abstract

          Background

          Babesia microti is an emerging tick-borne pathogen and the causative agent of human babesiosis. Mathematical modeling of the reproductive rate of B. microti indicates that it cannot persist in nature by horizontal tick-host transmission alone. We hypothesized that transplacental transmission in the reservoir population contributes to B. microti persistence and emergence in North American rodent populations.

          Methods

          Peromyscus leucopus were collected from Connecticut and Block Island, Rhode Island and analyzed using a highly specific quantitative PCR (qPCR) assay for infection with B. microti.

          Results

          In April, 100% ( n = 103) of mice were infected with B. microti. Females exhibited significantly higher parasitemia than their offspring ( P < 0.0001) and transplacental transmission was observed in 74.2% of embryos ( n = 89). Transplacental transmission of B. microti is thus a viable and potentially important infectious pathway in naturally infected rodent species and should be considered in future theoretical and empirical studies.

          Conclusions

          To our knowledge, this study is the first to report transplacental transmission of B. microti occurring in its natural reservoir host, P. leucopus, in the United States and the only study that provides a quantitative estimate of parasitemia. This vector-independent pathway could contribute to the increased geographic range of B. microti or increase its abundance in endemic areas.

          Electronic supplementary material

          The online version of this article (10.1186/s13071-018-2875-8) contains supplementary material, which is available to authorized users.

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          Most cited references49

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          Biological consequences of global warming: is the signal already apparent?

          Increasing greenhouse gas concentrations are expected to have significant impacts on the world's climate on a timescale of decades to centuries. Evidence from long-term monitoring studies is now accumulating and suggests that the climate of the past few decades is anomalous compared with past climate variation, and that recent climatic and atmospheric trends are already affecting species physiology, distribution and phenology.
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            Coinfection by Ixodes Tick-Borne Pathogens: Ecological, Epidemiological, and Clinical Consequences.

            Ixodes ticks maintain a large and diverse array of human pathogens in the enzootic cycle, including Borrelia burgdorferi and Babesia microti. Despite the poor ecological fitness of B. microti, babesiosis has recently emerged in areas endemic for Lyme disease. Studies in ticks, reservoir hosts, and humans indicate that coinfection with B. burgdorferi and B. microti is common, promotes transmission and emergence of B. microti in the enzootic cycle, and causes greater disease severity and duration in humans. These interdisciplinary studies may serve as a paradigm for the study of other vector-borne coinfections. Identifying ecological drivers of pathogen emergence and host factors that fuel disease severity in coinfected individuals will help guide the design of effective preventative and therapeutic strategies.
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              Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species.

              The Lyme borreliosis agent Borrelia burgdorferi and the relapsing fever group species Borrelia miyamotoi co-occur in the United States. We used species-specific, quantitative polymerase chain reaction to study both species in the blood and skin of Peromyscus leucopus mice and host-seeking Ixodes scapularis nymphs at a Connecticut site. Bacteremias with B. burgdorferi or B. miyamotoi were most prevalent during periods of greatest activity for nymphs or larvae, respectively. Whereas B. burgdorferi was 30-fold more frequent than B. miyamotoi in skin biopsies and mice had higher densities of B. burgdorferi densities in the skin than in the blood, B. miyamotoi densities were higher in blood than skin. In a survey of host-seeking nymphs in 11 northern states, infection prevalences for B. burgdorferi and B. miyamotoi averaged approximately 0.20 and approximately 0.02, respectively. Co-infections of P. leucopus or I. scapularis with both B. burgdorferi and B. miyamotoi were neither more nor less common than random expectations.
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                Author and article information

                Contributors
                dt2503@columbia.edu
                mad2256@columbia.edu
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                4 May 2018
                4 May 2018
                2018
                : 11
                : 286
                Affiliations
                ISNI 0000000419368729, GRID grid.21729.3f, Ecology, Evolution, and Environmental Biology Department, , Columbia University, ; New York, NY 10027 USA
                Article
                2875
                10.1186/s13071-018-2875-8
                5935994
                29728129
                d70ff61a-ad09-4ae2-a2f4-f916542c9e4c
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 1 February 2018
                : 26 April 2018
                Funding
                Funded by: National Institutes of Health (US)
                Award ID: R01 GM105246
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Parasitology
                ixodes scapularis,rodent,babesiosis,emerging disease,congenital transmission
                Parasitology
                ixodes scapularis, rodent, babesiosis, emerging disease, congenital transmission

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