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  • 1.
    Aase, Audun
    et al.
    Norwegian Institute Public Heatlh, Norway.
    Hajdusek, Ondrej
    Academic Science Czech Republic, Czech Republic.
    Oines, Oivind
    Norwegian Vet Institute, Norway.
    Quarsten, Hanne
    Sorlandet Hospital Health Enterprise, Norway.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Herstad, Tove K.
    Norwegian Institute Public Heatlh, Norway.
    Kjelland, Vivian
    University of Agder, Norway; Sorlandet Hospital Health Enterprise, Norway.
    Sima, Radek
    Academic Science Czech Republic, Czech Republic.
    Jalovecka, Marie
    Academic Science Czech Republic, Czech Republic.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. County Hospital Ryhov, Sweden.
    Aaberge, Ingeborg S.
    Norwegian Institute Public Heatlh, Norway.
    Validate or falsify: Lessons learned from a microscopy method claimed to be useful for detecting Borrelia and Babesia organisms in human blood2016In: INFECTIOUS DISEASES, ISSN 2374-4235, Vol. 48, no 6, p. 411-419Article in journal (Refereed)
    Abstract [en]

    Background A modified microscopy protocol (the LM-method) was used to demonstrate what was interpreted as Borrelia spirochetes and later also Babesia sp., in peripheral blood from patients. The method gained much publicity, but was not validated prior to publication, which became the purpose of this study using appropriate scientific methodology, including a control group. Methods Blood from 21 patients previously interpreted as positive for Borrelia and/or Babesia infection by the LM-method and 41 healthy controls without known history of tick bite were collected, blinded and analysed for these pathogens by microscopy in two laboratories by the LM-method and conventional method, respectively, by PCR methods in five laboratories and by serology in one laboratory. Results Microscopy by the LM-method identified structures claimed to be Borrelia- and/or Babesia in 66% of the blood samples of the patient group and in 85% in the healthy control group. Microscopy by the conventional method for Babesia only did not identify Babesia in any samples. PCR analysis detected Borrelia DNA in one sample of the patient group and in eight samples of the control group; whereas Babesia DNA was not detected in any of the blood samples using molecular methods. Conclusions The structures interpreted as Borrelia and Babesia by the LM-method could not be verified by PCR. The method was, thus, falsified. This study underlines the importance of doing proper test validation before new or modified assays are introduced.

  • 2.
    Adams, Yvonne
    et al.
    Univ Copenhagen, Denmark.
    Clausen, Anne Skovsbo
    Copenhagen Univ Hosp, Denmark; Copenhagen Univ Hosp, Denmark.
    Jensen, Peter Ostrup
    Lager, Malin
    Linköping University, Department of Biomedical and Clinical Sciences. Linköping University, Faculty of Medicine and Health Sciences. Natl Reference Lab Borrel, Div Clin Microbiol, Other Tick Borne Bacter, Lab Med, Reg Jonkoping Cty, Jonkoping, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Natl Reference Lab Borrel, Div Clin Microbiol, Other Tick Borne Bacter, Lab Med, Reg Jonkoping Cty, Jonkoping, Sweden.
    Jonsson Henningsson, Anna
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Center for Diagnostics, Department of Clinical Microbiology. Natl Reference Lab Borrel, Div Clin Microbiol, Other Tick Borne Bacter, Lab Med, Reg Jonkoping Cty, Jonkoping, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Natl Reference Lab Borrel, Div Clin Microbiol, Other Tick Borne Bacter, Lab Med, Reg Jonkoping Cty, Jonkoping, Sweden.
    Faurholt-Jepsen, Daniel
    Copenhagen Univ Hosp, Denmark.
    Mens, Helene
    Copenhagen Univ Hosp, Denmark.
    Kraiczy, Peter
    Goethe Univ Frankfurt, Germany.
    Kragh, Kasper Norskov
    Copenhagen Univ Hosp, Denmark; Univ Copenhagen, Denmark.
    Bjarnsholt, Thomas
    Copenhagen Univ Hosp, Denmark; Univ Copenhagen, Denmark.
    Kjaer, Andreas
    Copenhagen Univ Hosp, Denmark; Copenhagen Univ Hosp, Denmark.
    Lebech, Anne-Mette
    Copenhagen Univ Hosp, Denmark; Univ Copenhagen, Denmark.
    Jensen, Anja R.
    Univ Copenhagen, Denmark.
    3D blood-brain barrier-organoids as a model for Lyme neuroborreliosis highlighting genospecies dependent organotropism2023In: ISCIENCE, ISSN 2589-0042, Vol. 26, no 1, article id 105838Article in journal (Refereed)
    Abstract [en]

    Lyme neuroborreliosis (LNB), a tick-borne infection caused by spirochetes within the Borrelia burgdorferi sensu lato (s.L.) complex, is among the most prevalent bacterial central nervous system (CNS) infections in Europe and the US. Here we have screened a panel of low- passage B. burgdorferi s.l. isolates using a novel, human-derived 3D blood-brain barrier (BBB)-organoid model. We show that human-derived BBB-organoids support the entry of Borrelia spirochetes, leading to swelling of the organoids and a loss of their structural integrity. The use of the BBB-organoid model highlights the organotropism between B. burgdorferi s.l. genospecies and their ability to cross the BBB contributing to CNS infection.

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  • 3.
    Carlströmer Berthén, Nellie
    et al.
    Borrelia Research Group of the Aland Islands, The Aland Islands, Finland; Bimelix AB, The Aland Islands, Finland.
    Tompa, Eszter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    Olausson, Susanne
    Borrelia Research Group of the Aland Islands,The Aland Islands, Finland;Bimelix AB, The Aland Islands, Finland.
    Nyberg, Clara
    Borrelia Research Group of the Aland Islands, The Aland Islands, Finland.
    Nyman, Dag
    Borrelia Research Group of the Aland Islands, The Aland Islands, Finland;Bimelix AB, The Aland Islands, Finland.
    Ringbom, Malin
    Borrelia Research Group of the Aland Islands, The Aland Islands, Finland;The Aland Islands Healthcare Services, The Aland Islands, Finland.
    Perander, Linda
    Borrelia Research Group of the Aland Islands, The Aland Islands, Finland;The Aland Islands Healthcare Services, The Aland Islands, Finland.
    Svärd, Joel
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Clinical Microbiology, Laboratory Medicine, County Hospital Ryhov, Sweden.
    Forsberg, Pia
    Linköping University, Faculty of Medicine and Health Sciences. Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Clinical Microbiology, Laboratory Medicine, County Hospital Ryhov, 551 85 Jonkoping, Sweden.
    Sjöwall, Johanna
    Linköping University, Faculty of Medicine and Health Sciences. Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Region Östergötland, Medicine Center, Department of Infectious Diseases.
    Nordberg, Marika
    Borrelia Research Group of the Aland Island, The Aland Islands, Finland;The Aland Islands Healthcare Services, The Aland Islands, Finland.
    The AxBioTick Study: Borrelia Species and Tick-Borne Encephalitis Virus in Ticks, and Clinical Responses in Tick-Bitten Individuals on the Aland Islands, Finland2023In: Microorganisms, E-ISSN 2076-2607, Vol. 11, no 5, article id 1100Article in journal (Refereed)
    Abstract [en]

    The AxBioTick Study: Borrelia Species and Tick-Borne Encephalitis Virus in Ticks, and Clinical Responses in Tick-Bitten Individuals on the Aland Islands, Finlandby  Nellie Carlströmer Berthén 1,2,*,† , Eszter Tompa 3,† , Susanne Olausson 1,2, Clara Nyberg 1, Dag Nyman 1,2, Malin Ringbom 1,4, Linda Perander 1,4, Joel Svärd 3, Per-Eric Lindgren 3,5, Pia Forsberg 3, Peter Wilhelmsson 3,5,‡, Johanna Sjöwall 3,6,‡  and Marika Nordberg 1,4,‡  1Borrelia Research Group of the Aland Islands, 22100 Mariehamn, The Aland Islands, Finland2Bimelix AB, 22100 Mariehamn, The Aland Islands, Finland3Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection, Linkoping University, 581 83 Linkoping, Sweden4The Aland Islands Healthcare Services, 22100 Mariehamn, The Aland Islands, Finland5Clinical Microbiology, Laboratory Medicine, County Hospital Ryhov, 551 85 Jonkoping, Sweden6Department of Infectious Diseases, Vrinnevi Hospital, 603 79 Norrkoping, Sweden*Author to whom correspondence should be addressed.†These authors contributed equally to the study.‡These authors contributed equally to the study.Microorganisms 2023, 11(5), 1100; https://doi.org/10.3390/microorganisms11051100Received: 30 March 2023 / Revised: 17 April 2023 / Accepted: 19 April 2023 / Published: 22 April 2023(This article belongs to the Special Issue Research on Ticks and Tick-Borne Pathogens)

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    AbstractThe AxBioTick study was initiated to investigate the prevalence of ticks and tick-borne pathogens and their impact on antibody and clinical responses in tick-bitten individuals on the Aland Islands. This geographical area is hyperendemic for both Lyme borreliosis (LB) and Tick-borne encephalitis (TBE). Blood samples and ticks were collected from 100 tick-bitten volunteers. A total of 425 ticks was collected, all determined to Ixodes ricinus using molecular tools. Of them 20% contained Borrelia species, of which B. garinii and B. afzelii were most common. None contained the TBE virus (TBEV). Blood samples were drawn in conjunction with the tick bite, and eight weeks later. Sera were analyzed for Borrelia- and TBEV-specific antibodies using an ELISA and a semiquantitative antibody assay. In total 14% seroconverted in Borrelia C6IgG1, 3% in TBEV IgG, and 2% in TBEV IgM. Five participants developed clinical manifestations of LB. The high seroprevalence of both Borrelia (57%) and TBEV (52%) antibodies are likely attributed to the endemic status of the corresponding infections as well as the TBE vaccination program. Despite the similar prevalence of Borrelia spp. detected in ticks in other parts of Europe, the infection rate in this population is high. The AxBioTick study is continuing to investigate more participants and ticks for co-infections, and to characterize the dermal immune response following a tick bite.

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  • 4.
    Chiappa, Giulia
    et al.
    Univ Milan, Italy.
    Perini, Matteo
    Univ Milan, Italy.
    Cafiso, Alessandra
    Univ Milan, Italy.
    Nodari, Riccardo
    Univ Milan, Italy.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Sweden.
    Omazic, Anna
    Natl Vet Inst, Sweden.
    Ullman, Karin
    Natl Vet Inst, Sweden.
    Moutailler, Sara
    Ecole Natl Vet Alfort, France.
    Kjellander, Petter
    Swedish Univ Agr Sci, Sweden.
    Bazzocchi, Chiara
    Univ Milan, Italy.
    Grandi, Giulio
    Natl Vet Inst, Sweden; Swedish Univ Agr Sci, Sweden.
    A Novel High Discriminatory Protocol for the Detection of Borrelia afzelii, Borrelia burgdorferi Sensu Stricto and Borrelia garinii in Ticks2022In: Pathogens, E-ISSN 2076-0817, Vol. 11, no 11, article id 1234Article in journal (Refereed)
    Abstract [en]

    Bacteria of the Borrelia burgdorferi sensu lato complex are the causative agents of Lyme borreliosis (LB). Even if the conventional diagnosis of LB does not rely on the species itself, an accurate species identification within the complex will provide a deepened epidemiological scenario, a better diagnosis leading to a more targeted therapeutic approach, as well as promote the general publics awareness. A comparative genomics approach based on the 210 Borrelia spp. genomes available in 2019 were used to set up three species-specific PCR protocols, able to detect and provide species typing of Borrelia afzelii, Borrelia burgdorferi sensu stricto (s.s.) and Borrelia garinii, the three most common and important human pathogenic Lyme Borrelia species in Europe. The species-specificity of these protocols was confirmed on previously identified B. afzelii, B. burgdorferi s.s. and B. garinii specimens detected in Ixodes ricinus samples. In addition, the protocols were validated on 120 DNA samples from ticks collected in Sweden, showing 88% accuracy, 100% precision, 72% sensitivity and 100% specificity. The proposed approach represents an innovative tool in epidemiological studies focused on B. burgdorferi s.l. occurrence in ticks, and future studies could suggest its helpfulness in routine diagnostic tests for health care.

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  • 5.
    Cronhjort, Samuel
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Department of Clinical Microbiology, Jönköping, Sweden.
    Karlsson, Linda
    Division of CBRN Defence and Security, Swedish Defence Research Agency, Umeå, Sweden.
    Thelaus, Johanna
    Division of CBRN Defence and Security, Swedish Defence Research Agency, Umeå, Sweden.
    Sjödin, Andreas
    Division of CBRN Defence and Security, Swedish Defence Research Agency, Umeå, Sweden.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Department of Clinical Microbiology, Jönköping, Sweden.
    The Tick-Borne Diseases STING study: Real-time PCR analysis of three emerging tick-borne pathogens in ticks that have bitten humans in different regions of Sweden and the Aland islands, Finland2019In: Infection Ecology & Epidemiology, ISSN 2000-8686, E-ISSN 2000-8686, Vol. 9, no 1, article id 1683935Article in journal (Refereed)
    Abstract [en]

    A milder climate has during the last decade contributed to an increased density and spreading of ixodid ticks, thus enhancing their role as emerging vectors for pathogenic microorganisms in northern Europe. It remains unclear if they contribute to the occurrence of infections caused by the bacteria Bartonella spp., Francisella tularensis subspecies holarctica and the parasite Toxoplasma gondii in Sweden and on the Åland islands, Finland. In this study, we want to improve understanding of the tick-borne transmission of these pathogens. Volunteers were recruited at primary healthcare centers. Ticks and blood samples were acquired from participants recruited in 2008 and 2009. Health questionnaires were completed, and medical records were acquired where applicable. Feeding time was estimated and screening of pathogens in the ticks was performed through real-time PCR. Ticks (n = 1849) were of mixed developmental stages: 76 larvae, 1295 nymphs, 426 adults and 52 undetermined. All analyzed ticks were considered negative for these pathogens since the CT-values were all below the detection limit for Bartonella spp. (1663 ticks), Francisella spp. (1849 ticks) and Toxoplasma gondii (1813 ticks). We assume that infections with these pathogens are caused by other transmission pathways within these regions of Sweden and the Åland islands, Finland.

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  • 6.
    Dessau, Ram B
    et al.
    Slagelse Hospital, Slagelse, Denmark.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Ekerfelt, Christina
    Linköping University, Department of Clinical and Experimental Medicine, Division of Neuro and Inflammation Science. Linköping University, Faculty of Medicine and Health Sciences.
    Nyman, Dag
    Åland University, Mariehamn, Finlad.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Study of a Cohort of 1,886 Persons To Determine Changes in Antibody Reactivity to Borrelia burgdorferi 3 Months after a Tick Bite2015In: Clinical and Vaccine Immunology, ISSN 1556-6811, E-ISSN 1556-679X, Vol. 22, no 7, p. 823-827Article in journal (Refereed)
    Abstract [en]

    Lyme borreliosis is a tick-borne disease caused by the bacterium Borrelia burgdorferi. The most frequent clinical manifestation is a rash called erythema migrans. Changes in antibody reactivity to B. burgdorferi 3 months after a tick bite are measured using enzyme-linked immunosorbent assays (ELISAs). One assay is based on native purified flagellum antigen (IgG), and the other assay is based on a recombinant antigen called C6 (IgG or IgM). Paired samples were taken at the time of a tick bite and 3 months later from 1,886 persons in Sweden and the Åland Islands, Finland. The seroconversion or relative change is defined by dividing the measurement units from the second sample by those from the first sample. The threshold for the minimum level of significant change was defined at the 2.5% level to represent the random error level. The thresholds were a 2.7-fold rise for the flagellar IgG assay and a 1.8-fold rise for the C6 assay. Of 1,886 persons, 102/101 (5.4%) had a significant rise in antibody reactivity in the flagellar assay or the C6 assay. Among 40 cases with a diagnosis of Lyme borreliosis, the sensitivities corresponding to a rise in antibodies were 33% and 50% for the flagellar antigen and the C6 antigen, respectively. Graphical methods to display the antibody response and to choose thresholds for a rise in relative antibody reactivity are shown and discussed. In conclusion, 5.4% of people with tick bites showed a rise in Borrelia-specific antibodies above the 2.5% threshold in either ELISA but only 40 (2.1%) developed clinical Lyme borreliosis.

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  • 7.
    Eliassen, Knut Eirik
    et al.
    Univ Bergen, Norway.
    Ocias, Lukas Frans
    Statens Serum Inst, Denmark; Karlstad Hosp, Sweden.
    Krogfelt, Karen A.
    Statens Serum Inst, Denmark; Roskilde Univ, Denmark.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Dudman, Susanne Gjeruldsen
    Univ Oslo, Norway; Oslo Univ Hosp, Norway.
    Andreassen, Åshild
    Norwegian Inst Publ Hlth, Norway; Univ South Eastern Norway, Norway.
    Lindbak, Morten
    Univ Oslo, Norway.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Tick-transmitted co-infections among erythema migrans patients in a general practice setting in Norway: a clinical and laboratory follow-up study2021In: BMC Infectious Diseases, E-ISSN 1471-2334, Vol. 21, no 1, article id 1044Article in journal (Refereed)
    Abstract [en]

    Background Erythema migrans (EM) is the most common manifestation of Lyme borreliosis. Here, we examined EM patients in Norwegian general practice to find the proportion exposed to tick-transmitted microorganisms other than Borrelia, and the impact of co-infection on the clinical manifestations and disease duration. Methods Skin biopsies from 139/188 EM patients were analyzed using PCR for Neoehrlichia mikurensis, Rickettsia spp., Anaplasma phagocytophilum and Babesia spp. Follow-up sera from 135/188 patients were analyzed for spotted fever group (SFG) Rickettsia, A. phagocytophilum and Babesia microti antibodies, and tested with PCR if positive. Day 0 sera from patients with fever (8/188) or EM duration of >= 21 days (69/188) were analyzed, using PCR, for A. phagocytophilum, Rickettsia spp., Babesia spp. and N. mikurensis. Day 14 sera were tested for TBEV IgG. Results We detected no microorganisms in the skin biopsies nor in the sera of patients with fever or prolonged EM duration. Serological signs of exposure against SFG Rickettsia and A. phagocytophilum were detected in 11/135 and 8/135, respectively. Three patients exhibited both SFG Rickettsia and A. phagocytophilum antibodies, albeit negative PCR. No antibodies were detected against B. microti. 2/187 had TBEV antibodies without prior immunization. There was no significant increase in clinical symptoms or disease duration in patients with possible co-infection. Conclusions Co-infection with N. mikurensis, A. phagocytophilum, SFG Rickettsia, Babesia spp. and TBEV is uncommon in Norwegian EM patients. Despite detecting antibodies against SFG Rickettsia and A. phagocytophilum in some patients, no clinical implications could be demonstrated.

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  • 8.
    Eskeland, Sveinung
    et al.
    Norwegian Univ Life Sci, Norway.
    Stuen, Snorre
    Norwegian Univ Life Sci, Norway.
    Crosby, Francy L.
    Univ Florida, FL 32608 USA.
    Lybeck, Kari
    Norwegian Vet Inst, Norway.
    Barbet, Anthony F.
    Univ Florida, FL 32608 USA.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences.
    Tollefsen, Stig
    Norwegian Vet Inst, Norway.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Tollersrud, Tore S.
    Norwegian Meat and Poultry Res Ctr, Norway.
    Makvandi-Nejad, Shokouh
    Norwegian Vet Inst, Norway.
    Granquist, Erik G.
    Norwegian Univ Life Sci, Norway.
    Assessing the clinical and bacteriological outcomes of vaccination with recombinant Asp14 and OmpA against A. phagocytophilum in sheep2019In: Veterinary Immunology and Immunopathology, ISSN 0165-2427, E-ISSN 1873-2534, Vol. 218, article id UNSP 109936Article in journal (Refereed)
    Abstract [en]

    Anaplasma phagocytophilum is a tick borne bacterium, causing disease in sheep and other mammals, including humans. The bacterium has great economic and animal welfare implications for sheep husbandry in Northern Europe. With the prospect of a warmer and more humid climate, the vector availability will likely increase, resulting in a higher prevalence of A. phagocytophilum. The current preventive measures, as pyrethroids acting on ticks or long acting antibiotics controlling bacterial infection, are suboptimal for prevention of the disease in sheep. Recently, the increased awareness on antibiotic- and pyrethorid resistance, is driving the search for a new prophylactic approach in sheep against A. phagocytophilum. Previous studies have used an attenuated vaccine, which gave insufficient protection from challenge with live bacteria. Other studies have focused on bacterial membrane surface proteins like Asp14 and OmpA. An animal study using homologous proteins to Asp14 and OmpA of A. marginate, showed no protective effect in heifers. In the current study, recombinant proteins of Asp14 (rAsp14) and OmpA (rOmpA) of A. phagocytophilum were produced and prepared as a vaccine for sheep. Ten lambs were vaccinated twice with an adjuvant emulsified with rAsp14 or rOmpA, three weeks apart and challenged with a live strain of A. phagocytophilum (GenBank acc.nr M73220) on day 42. The control group consisted of five lambs injected twice with PBS and adjuvant. Hematology, real time qPCR, immunodiagnostics and flow cytometric analyses of peripheral blood mononuclear cells were performed. Vaccinated lambs responded with clinical signs of A.phagocytophilum infection after challenge and bacterial load in the vaccinated group was not reduced compared to the control group. rAsp14 vaccinated lambs generated an antibody response against the vaccine, but a clear specificity for rAsp14 could not be established. rOmpA-vaccinated lambs developed a strong specific antibody response on days 28 after vaccination and 14 days post-challenge. Immunofluorescent staining and flow cytometric analysis of peripheral blood mononuclear monocytes revealed no difference between the three groups, but the percentage of CD4, CD8(+), gamma delta TcR+, lambda-Light chain(+), CD11b(+), CD14(+) and MHC II+ cells, within the groups changed during the study, most likely due to the adjuvant or challenge with the bacterium. Although an antigen specific antibody response could be detected against rOmpA and possibly rAsp14, the vaccines seemed to be ineffective in reducing clinical signs and bacterial load caused by A. phagocytophilum. This is the first animal study with recombinant Asp14 and OmpA aimed at obtaining clinical protection against A. phagocytophilum in sheep.

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  • 9.
    Eskeland, Sveinung
    et al.
    Norwegian Univ Life Sci, Norway.
    Stuen, Snorre
    Norwegian Univ Life Sci, Norway.
    Munderloh, Ulrike G.
    Univ Minnesota, MN 55108 USA.
    Barbet, Anthony
    Univ Florida, FL 32608 USA.
    Crosby, Liliana
    Univ Florida, FL 32608 USA.
    Lybeck, Kari
    Norwegian Vet Inst, Norway.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Makvandi-Nejad, Shokouh
    Norwegian Vet Inst, Norway.
    Tollefsen, Stig
    Norwegian Vet Inst, Norway; Coalit Epidem Preparedness CEPI, Norway.
    Granquist, Erik G.
    Norwegian Univ Life Sci, Norway.
    Clinical and immunological responses in sheep after inoculation with Himar1-transformed Anaplasma phagocytophilum and subsequent challenge with a virulent strain of the bacterium2021In: Veterinary Immunology and Immunopathology, ISSN 0165-2427, E-ISSN 1873-2534, Vol. 231, article id 110165Article in journal (Refereed)
    Abstract [en]

    In Norway, the tick-transmitted bacterium Anaplasma phagocytophilum is estimated to cause tick-borne fever (TBF) in 300 000 lambs on pastures each year, resulting in economic and animal welfare consequences. Today, prophylactic measures mainly involve the use of acaricides, but a vaccine has been requested by farmers and veterinarians for decades. Several attempts have been made to produce a vaccine against A. phagocytophilum including antigenic surface proteins, inactivated whole cell vaccines and challenge followed by treatment. In the current study, a virulent wild type strain of A. phagocytophilum named Ap.Norvar1 (16S rRNA sequence partial identical to sequence in GenBank acc.no M73220) was subject to genetic transformation with a Himar1-transposon, which resulted in three bacterial mutants, capable of propagation in a tick cell line (ISE6). In order to test the immunogenicity and pathogenicity of the live, mutated bacteria, these were clinically tested in an inoculation- and challenge study in sheep. One group was inoculated with the Ap.Norvar1 as an infection control. After inoculation, the sheep inoculated with mutated bacteria and the Ap.Norvar1 developed typical clinical signs of infection and humoral immune response. After challenge with Ap.Norvar1, 28 days later all groups inoculated with mutated bacteria showed clinical signs of tick-borne fever and bacteremia while the group initially inoculated with the Ap.Norvar1, showed protection against clinical disease. The current study shows a weak, but partial protection against infection in animals inoculated with mutated bacteria, while animals that received Ap.Norvar1 both for inoculation and challenge, responded with homologues protection.

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  • 10.
    Fryland, Linda
    et al.
    Linköping University, Faculty of Health Sciences. Linköping University, Department of Clinical and Experimental Medicine, Clinical Immunology.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Infectious Diseases. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Centre for Medicine, Department of Infectious Diseases in Östergötland.
    Sandin, Linnea
    Linköping University, Department of Clinical and Experimental Medicine, Cell Biology. Linköping University, Faculty of Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Cell Biology. Linköping University, Faculty of Health Sciences.
    Lindblom, Pontus
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Nyman, Dag
    Aland Borrelia Grp.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Ernerudh, Jan
    Linköping University, Department of Clinical and Experimental Medicine, Clinical Immunology. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Centre for Laboratory Medicine, Department of Clinical Immunology and Transfusion Medicine.
    Ekerfelt, Christina
    Linköping University, Faculty of Health Sciences. Linköping University, Department of Clinical and Experimental Medicine, Clinical Immunology.
    Biomarkers in blood a few days after a bite by a Borrelia burgdorferi infected tick:: Asymptomatic Borrelia burgdorferi-infected subjects show higher Th1-associated response compared with subjects who later develop Lyme borreliosis2012Manuscript (preprint) (Other academic)
    Abstract [en]

    The clinical outcome following infection with Borrelia (B.) burgdorferi sensu lato (s.l.) differs between individuals, ranging from asymptomatic infection to Lyme borreliosis (LB) with persistent symptoms post-treatment. Previous studies in mice and humans have generated the hypothesis that a successful outcome of B. burgdorferi s.l. infection is associated with an early strong pro-inflammatory T helper (Th)1-like immune response. The aim of this study was to assess the early course of events in B. burgdorferi s.l.-associated inflammation by screening for possible early immune biomarkers in peripheral blood from newly tick-bitten persons. The study subjects bitten by B. burgdorferi s.l.-infected ticks were divided into (1) those later developing clinical LB, (2) those who developed anti-B. burgdorferi s.l. antibodies but not clinical LB, (3) those who neither developed antibodies nor clinical LB. A fourth group consisted of bitten study subjects without development of antibodies or clinical LB. Two sets of samples, both comprising all four groups, were collected in order to repeat the analyses and confirm the data. Sera or plasma collected a few days after the tick bite were analysed for 18 biomarkers (IL-1β, IL-6, CXCL8/IL-8, IL-12p70, IL-17A, IL-27, TNF, CCL18, CCL20, CCL22, CXCL1, CXCL9, CXCL10, CXCL11, calprotectin, MMP-3, MMP-8, MMP-9) by multiplex bead assay and ELISA. In the first set of samples, the neutrophil activation marker calprotectin was increased in subjects who developed clinical LB compared with subjects who developed antibodies against B. burgdorferi s.l. but did not develop LB. However, the finding could not be confirmed in the second set of samples, thus the study failed to identify an early prognostic marker for development of clinical LB. Interestingly, both sets of samples showed increases in two different Th1-associated markers, CXCL10 and IL-12p70, respectively, in subjects who following a bite by a B. burgdorferi s.l.-infected tick developed antibodies against B. burgdorferi s.l. but did not develop LB compared with subjects who developed clinical LB, thus supporting the hypothesis of an early strong Th1-response being important for optimal resolution of B. burgdorferi s.l. infection.

  • 11.
    Fryland, Linda
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Clinical Immunology. Linköping University, Faculty of Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Nyman, Dag
    Aland Borrelia Grp.
    Ekerfelt, Christina
    Linköping University, Department of Clinical and Experimental Medicine, Clinical Immunology. Linköping University, Faculty of Health Sciences.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Infectious Diseases. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Centre for Medicine, Department of Infectious Diseases in Östergötland.
    Low risk of developing Borrelia burgdorferi infection in the south-east of Sweden after being bitten by a Borrelia burgdorferi-infected tick2011In: INTERNATIONAL JOURNAL OF INFECTIOUS DISEASES, ISSN 1201-9712, Vol. 15, no 3, p. E174-E181Article in journal (Refereed)
    Abstract [en]

    Objectives: The risk of developing Lyme borreliosis (LB) from Borrelia burgdorferi sensu lato (Bb)-infected ticks in Sweden is largely unknown. In the current study, we investigated the prevalence of Bb in ticks that had bitten humans and the risk of developing LB from Bb-infected ticks. Methods: Health questionnaires, blood samples, and ticks were collected from 394 tick-bitten study subjects in the County of Ostergotland, Sweden, at the time of the tick bite. Questionnaires and blood samples were also collected 3 months later. Ticks were screened for Bb DNA with PCR, while sera were analyzed for antibodies against Bb using two ELISA assays. Seroconversion, i.e., an at least two-fold increase in anti-Bb antibodies after 3 months, was confirmed using a Strip-Immunoassay. Results: Seventy-five of 397 ticks collected from the study subjects were determined to be Bb-positive. Sixty-four of the tick-bitten subjects had been bitten by Bb-infected ticks. Four of them showed seroconversion and were therefore considered to have an active Bb infection. None of these four subjects had sought health care due to symptoms, but one reported symptoms. Conclusions: Our data suggest that the risk of developing LB after being bitten by a Bb-infected tick is low, and asymptomatic Bb infections appear to be more frequent than symptomatic infections.

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  • 12.
    Grankvist, Anna
    et al.
    University of Gothenburg, Sweden; Sahlgrens University Hospital, Sweden.
    Labbe Sandelin, Lisa
    Kalmar County Hospital, Sweden; Uppsala University, Sweden.
    Andersson, Jennie
    University of Gothenburg, Sweden; Sahlgrens University Hospital, Sweden.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. County Hospital Ryhov, Sweden.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Heart and Medicine Center, Department of Infectious Diseases.
    Wenneras, Christine
    University of Gothenburg, Sweden; Sahlgrens University Hospital, Sweden.
    Infections with Candidatus Neoehrlichia mikurensis and Cytokine Responses in 2 Persons Bitten by Ticks, Sweden2015In: Emerging Infectious Diseases, ISSN 1080-6040, E-ISSN 1080-6059, Vol. 21, no 8, p. 1462-1465Article in journal (Refereed)
    Abstract [en]

    The prevalence of Candidatus Neoehrlichia mikurensis infection was determined in 102 persons bitten by ticks in Sweden. Two infected women had erythematous rashes; 1 was co-infected with a Borrelia sp., and the other showed seroconversion for Anaplasma phagocytophilum. Both patients had increased levels of Neoehrlichia DNA and serum cytokines for several months.

  • 13.
    Gyllemark, Paula
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Infect Dis, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Sweden.
    Elm, Camilla
    Dept Clin Microbiol, Sweden.
    Hoornstra, Dieuwertje
    Univ Med Ctr Locat AMC, Netherlands.
    Hovius, Joppe W.
    Univ Med Ctr Locat AMC, Netherlands; European Soc Clin Microbiol & Infect Dis, Switzerland.
    Johansson, Marcus
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Jönköping,Sweden.
    Tjernberg, Ivar
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Chem & Transfus Med, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Sweden; European Soc Clin Microbiol & Infect Dis, Switzerland.
    Jonsson Henningsson, Anna
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Center for Diagnostics, Department of Clinical Microbiology. Dept Clin Microbiol, Sweden; European Soc Clin Microbiol & Infect Dis, Switzerland.
    Sjöwall, Johanna
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Medicine Center, Department of Infectious Diseases.
    Are other tick-borne infections overlooked in patients investigated for Lyme neuroborreliosis?: A large retrospective study from South-eastern Sweden2021In: Ticks and Tick-borne Diseases, ISSN 1877-959X, E-ISSN 1877-9603, Vol. 12, no 5, article id 101759Article in journal (Refereed)
    Abstract [en]

    In Europe, the hard tick Ixodes ricinus is considered the most important vector of human zoonotic diseases. Human pathogenic agents spread by I. ricinus in Sweden include Borrelia burgdorferi sensu lato (s.l.), Anaplasma phagocytophilum, Rickettsia helvetica, the recently described Neoehrlichia mikurensis, Borrelia miyamotoi, tick-borne encephalitis virus (TBEV), and Babesia spp. (Babesia microti, Babesia venatorum and Babesia divergens). Since these pathogens share the same vector, co-infections with more than one tick-borne pathogen may occur and thus complicate the diagnosis and clinical management of the patient due to possibly altered symptomatology. Borrelia burgdorferi s.l., TBEV and B. miyamotoi are well-known to cause infections of the central nervous system (CNS), whereas the abilities of other tick-borne pathogens to invade the CNS are largely unknown. The aim of this study was to investigate the presence and clinical impact of tick-borne pathogens other than B. burgdorferi s.l. in the cerebrospinal fluid (CSF) and serum samples of patients who were under investigation for Lyme neuroborreliosis (LNB) in a tick-endemic region of South-eastern Sweden. CSF and serum samples from 600 patients, recruited from the Regions of center dot Ostergo center dot tland County, Jo center dot nko center dot ping County and Kalmar County in South-eastern Sweden and investigated for LNB during the period of 2009-2013, were retrospectively collected for analysis. The samples were analysed by real-time PCR for the presence of nucleic acid from B. burgdorferi s.l., B. miyamotoi, A. phagocytophilum, Rickettsia spp., N. mikurensis, TBEV and Babesia spp. Serological analyses were conducted in CSF and serum samples for all patients regarding B. burgdorferi s.l., and for the patients with CSF mononuclear pleocytosis, analyses of antibodies to B. miyamotoi, A. phagocytophilum, spotted fever group (SFG) rickettsiae, TBEV and B. microti in serum were performed. The medical charts of all the patients with CSF mononuclear pleocytosis and patients with positive PCR findings were reviewed. Of the 600 patients, 55 (9%) presented with CSF mononuclear pleocytosis, 13 (2%) of whom had Borrelia-specific antibodies in the CSF. One patient was PCRpositive for N. mikurensis, and another one was PCR-positive for Borrelia spp. in serum. No pathogens were detected by PCR in the CSF samples. Four patients had serum antibodies to B. miyamotoi, four patients to A. phagocytophilum, five patients to SFG rickettsiae, and six patients to TBEV. One patient, with antibodies to SFG

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  • 14.
    Henningsson, Anna
    et al.
    Ryhov County Hospital, Jönköping.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Gyllemark, Paula
    Ryhov County Hospital, Jönköping.
    Kozak Ljunggren, Monika
    Linköping University, Faculty of Medicine and Health Sciences. Linköping University, Department of Clinical and Experimental Medicine, Division of Cell Biology.
    Matussek, Andreas
    Ryhov County Hospital, Jönköping.
    Nyman, Dag
    Ryhov County Hospital, Jönköping.
    Ekerfelt, Christina
    Bimelix Biomedical Laboratory, Mariehamn, Åland, Finland .
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Ryhov County Hospital, Jönköping.
    Forsberg, Pia
    Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Heart and Medicine Center, Department of Infectious Diseases. Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine.
    Low risk of seroconversion or clinical disease in humans after a bite by an Anaplasma phagocytophilum-infected tick2015In: Ticks and Tick-borne Diseases, ISSN 1877-959X, E-ISSN 1877-9603, Vol. 6, no 6, p. 787-792Article in journal (Refereed)
    Abstract [en]

    The risk of contracting human granulocytic anaplasmosis (HGA) after a tick bite is mainly unknown. In this study we investigated the clinical and serological response in 30 humans bitten by ticks positive for Anaplasma phagocytophilum (Group A), 30 humans bitten by Borrelia burgdorferi sensu lato (s.l.)-positive ticks (Group B), and 30 humans bitten by ticks negative for both A. phagocytophilum and B. burgdorferi s.l. (Group C). Ticks, blood samples and questionnaires were collected from tick-bitten humans at 34 primary healthcare centres in Sweden and in the Åland Islands, Finland, at the time of the tick bite and after three months. A total of 2553 ticks detached from humans in 2007-2009 were analyzed by polymerase chain reaction, and 31 (1.2%) were positive for A. phagocytophilum, 556 (21.8%) were positive for B. burgdorferi s.l., and eight (0.3%) were co-infected by A. phagocytophilum and B. burgdorferi s.l. The overall prevalence of Anaplasma IgG antibodies in the included participants (n=90) was 17%, and there was no significant difference between the groups A-C. Only one of the participants (in Group C) showed a four-fold increase of IgG antibodies against A. phagocytophilum at the three-month follow-up, but reported no symptoms. The frequency of reported symptoms did not differ between groups A-C, and was unrelated to the findings of A. phagocytophilum and B. burgdorferi s.l. in the detached ticks. We conclude that the risk for HGA or asymptomatic seroconversion after a tick bite in Sweden or in the Åland Islands is low, even if the tick is infected by A. phagocytophilum.

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  • 15.
    Hoffman, Tove
    et al.
    Uppsala Univ, Sweden.
    Sjödin, Andreas
    Swedish Def Res Agcy, Sweden.
    Öhrman, Caroline
    Swedish Def Res Agcy, Sweden.
    Karlsson, Linda
    Swedish Def Res Agcy, Sweden.
    McDonough, Ryelan Francis
    No Arizona Univ, AZ 86011 USA.
    Sahl, Jason W.
    No Arizona Univ, AZ 86011 USA.
    Birdsell, Dawn
    No Arizona Univ, AZ 86011 USA.
    Wagner, David M.
    No Arizona Univ, AZ 86011 USA.
    Carra, Laura G.
    Uppsala Univ, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Pettersson, John H-O
    Uppsala Univ, Sweden; Univ Sydney, Australia; Univ Sydney, Australia.
    Barboutis, Christos
    Hellen Ornithol Soc, Greece.
    Figuerola, Jordi
    CSIC, Spain; CIBER Epidemiol & Salud Publ CIBERESP, Spain.
    Onrubia, Alejandro
    Migres Fdn, Spain.
    Kiat, Yosef
    Soc Protect Nat Israel SPNI, Israel.
    Piacentini, Dario
    Via Cesare Lippi 35, Italy.
    Jaenson, Thomas G. T.
    Uppsala Univ, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Moutailler, Sara
    Ecole Natl Vet Alfort, France.
    Fransson, Thord
    Swedish Museum Nat Hist, Sweden.
    Forsman, Mats
    Swedish Def Res Agcy, Sweden.
    Nilsson, Kenneth
    Uppsala Univ, Sweden.
    Lundkvist, Ake
    Uppsala Univ, Sweden.
    Olsen, Bjorn
    Uppsala Univ, Sweden.
    Co-Occurrence of Francisella, Spotted Fever Group Rickettsia, and Midichloria in Avian-Associated Hyalomma rufipes2022In: Microorganisms, E-ISSN 2076-2607, Vol. 10, no 7, article id 1393Article in journal (Refereed)
    Abstract [en]

    The migratory behavior of wild birds contributes to the geographical spread of ticks and their microorganisms. In this study, we aimed to investigate the dispersal and co-occurrence of Francisella and spotted fever group Rickettsia (SFGR) in ticks infesting birds migrating northward in the African-Western Palaearctic region (AWPR). Birds were trapped with mist nests across the Mediterranean basin during the 2014 and 2015 spring migration. In total, 575 ticks were collected from 244 birds. We screened the ticks for the species Francisella tularensis, the genus Francisella, and SFGR by microfluidic real-time PCR. Confirmatory analyses and metagenomic sequencing were performed on tick samples that putatively tested positive for F. tularensis during initial screenings. Hyalomma rufipes was the most common tick species and had a high prevalence of Francisella, including co-occurrence of Francisella and SFGR. Metagenomic analysis of total DNA extracted from two H. rufipes confirmed the presence of Francisella, Rickettsia, and Midichloria. Average nucleotide identity and phylogenetic inference indicated the highest identity of the metagenome-assembled genomes to a Francisella-like endosymbiont (FLE), Rickettsia aeschlimannii, and Midichloria mitochondrii. The results of this study suggest that (i) FLE- and SFGR-containing ticks are dispersed by northbound migratory birds in the AWPR, (ii) H. rufipes likely is not involved in transmission of F. tularensis in the AWPR, and (iii) a dual endosymbiosis of FLEs and Midichloria may support some of the nutritional requirements of H. rufipes.

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  • 16.
    Hoffman, Tove
    et al.
    Department of Medical Biochemistry and Microbiology (IMBIM), Zoonosis Science Center, Uppsala University, Uppsala, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Department of Clinical Microbiology, County Hospital Ryhov, Jönköping, Sweden.
    Barboutis, Christos
    Antikythira Bird Observatory, Hellenic Ornithological Society/Birdlife Greece, Athens, Greece.
    Fransson, Thord
    Department of Environmental Research and Monitoring, Swedish Museum of Natural History, Stockholm, Sweden.
    Jaenson, Thomas G T
    Department of Organismal Biology, Uppsala University, Uppsala, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Department of Clinical Microbiology, County Hospital Ryhov, Jönköping, Sweden.
    Von Loewenich, Friederike D.
    Department of Medical Microbiology and Hygiene, University of Mainz, Mainz, Germany.
    Lundkvist, Åke
    Department of Medical Biochemistry and Microbiology (IMBIM), Zoonosis Science Center, Uppsala University, Uppsala, Sweden.
    Olsen, Björn
    Department of Medical Sciences, Zoonosis Science Center, Uppsala University, Uppsala, Sweden.
    Salaneck, Erik
    Department of Medical Sciences, Zoonosis Science Center, Uppsala University, Uppsala, Sweden.
    A divergent Anaplasma phagocytophilum variant in an Ixodes tick from a migratory bird; Mediterranean basin2020In: Infection Ecology & Epidemiology, ISSN 2000-8686, E-ISSN 2000-8686, Vol. 10, no 1, article id 1729653Article in journal (Refereed)
    Abstract [en]

    Anaplasma phagocytophilum (AP) has vast geographical and host ranges and causes disease in humans and domesticated animals. We investigated the role of northward migratory birds in the dispersal of tick-borne AP in the African-Western Palearctic. Ticks were collected from northward migratory birds trapped during spring migration of 2010 at two localities in the central Mediterranean Sea. AP DNA was detected by PCR (gltA and 16S rRNA) and variant determination was performed using ankA sequences. In total, 358 ticks were collected. One of 19 ticks determined as Ixodes was confirmed positive for AP DNA. The tick was collected from a woodchat shrike (Lanius senator senator) trapped in Greece, and molecularly determined to belong to the I. ricinus complex and sharing highest (95%) 16S RNA sequence identity to I. gibbosus. The ankA AP sequence exhibited highest similarity to sequences from rodents and shrews (82%) and ruminants (80%). Phylogenetic analyses placed it convincingly outside other clades, suggesting that it represents a novel AP variant. The divergent Ixodes species harboring a novel AP variant could either indicate an enzootic cycle involving co-evolution with birds, or dissemination from other regions by avian migration. None of the 331 Hyalomma marginatum sensu lato ticks, all immature stages, were positive for AP DNA, lending no evidence for the involvement of Hyalomma ticks transported by birds in the ecology of AP.

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  • 17.
    Hvidsten, D.
    et al.
    Univ Hosp North Norway, Norway; Nordland Hosp, Norway.
    Frafjord, K.
    UiT Arctic Univ Norway, Norway.
    Gray, J. S.
    Univ Coll Dublin, Ireland.
    Jonsson Henningsson, Anna
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Clinical Microbiology, Region Jönköping County, Sweden.
    Jenkins, A.
    Univ South Eastern Norway, Norway.
    Kristiansen, B. E.
    Skiensgate 21, Norway.
    Lager, Malin
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Department of Clinical Microbiology, Region Jönköping County, Sweden.
    Rognerud, B.
    Univ Oslo, Norway.
    Slatsve, A. M.
    Nordland Hosp, Norway.
    Stordal, F.
    Univ Oslo, Norway.
    Stuen, S.
    Norwegian Univ Life Sci, Norway.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    The distribution limit of the common tick, Ixodes ricinus, and some associated pathogens in north-western Europe2020In: Ticks and Tick-borne Diseases, ISSN 1877-959X, E-ISSN 1877-9603, Vol. 11, no 4, article id 101388Article in journal (Refereed)
    Abstract [en]

    In north-western Europe, the common tick, Ixodes ricinus, is widely established, its distribution appears to be increasing and the spread of tick-borne diseases is of increasing concern. The project Flatt i Nord (Ticks in northern Norway) commenced in spring 2009 with the intention of studying the ticks distribution and that of its pathogens in northern Norway. Several methods were used: cloth-dragging, collecting from trapped small mammals, and collecting from pets. Since 2010, the occurrence of ticks in the region of northern Norway was determined directly by cloth-dragging 167 times in 109 separate locations between the latitudes of 64 degrees N and 70 degrees N (included seven locations in the northern part of Trondelag County). The northernmost location of a permanent I. ricinus population was found to be Nordoyvagen (66.2204 degrees N, 12.59 degrees E) on the Island of Donna. In a sample of 518 nymphal and adult ticks, the Borrelia prevalence collected close to this distribution limit varied but was low (1-15 %) compared with the locations in Trondelag, south of the study area (15-27 %). Five specimens (1 %) were positive for Rickettsia helvetica. The length of the vegetation growing season (GSL) can be used as an approximate index for the presence of established populations of I. ricinus. The present study suggests that the threshold GSL for tick establishment is about 170 days, because the median GSL from 1991 to 2015 was 174-184 days at sites with permanent tick populations, showing a clear increase compared with the period 1961-1990. This apparent manifestation of climate change could explain the northward extension of the range of I. ricinus.

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  • 18.
    Jaenson, Thomas G. T.
    et al.
    Uppsala Univ, Sweden.
    Gray, Jeremy S.
    Univ Coll Dublin, Ireland.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Coinfection of <i>Babesia</i> and <i>Borrelia</i> in the Tick <i>Ixodes ricinus</i>-A Neglected Public Health Issue in Europe?2024In: Pathogens, E-ISSN 2076-0817, Vol. 13, no 1, article id 81Article, review/survey (Refereed)
    Abstract [en]

    Ixodes ricinus nymphs and adults removed from humans, and larvae and nymphs from birds, have been analysed for infection with Babesia species and Borrelia species previously in separately published studies. Here, we use the same data set to explore the coinfection pattern of Babesia and Borrelia species in the ticks. We also provide an overview of the ecology and potential public health importance in Sweden of I. ricinus infected both with zoonotic Babesia and Borrelia species. Among 1952 nymphs and adult ticks removed from humans, 3.1% were PCR-positive for Babesia spp. Of these Babesia-positive ticks, 43% were simultaneously Borrelia-positive. Among 1046 immatures of I. ricinus removed from birds, 2.5% were Babesia-positive, of which 38% were coinfected with Borrelia species. This study shows that in I. ricinus infesting humans or birds in Sweden, potentially zoonotic Babesia protozoa sometimes co-occur with human-pathogenic Borrelia spp. Diagnostic tests for Babesia spp. infection are rarely performed in Europe, and the medical significance of this pathogen in Europe could be underestimated.

  • 19.
    Jaenson, Thomas G. T.
    et al.
    Uppsala Univ, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    First Record of a Suspected Human-Pathogenic Borrelia Species in Populations of the Bat Tick Carios vespertilionis in Sweden2021In: Microorganisms, E-ISSN 2076-2607, Vol. 9, no 5, article id 1100Article in journal (Refereed)
    Abstract [en]

    The bat tick Carios vespertilionis has been reported from Sweden to occasionally feed on humans resulting in disease symptoms. The aim of this study was to investigate C. vespertilionis as a potential vector and reservoir of Borrelia species. In 2015 and 2018 in south-central Sweden, C. vespertilionis ticks were collected from a wooden bat box harboring Soprano pipistrelle bats, Pipistrellus pygmaeus. In addition, one C. vespertilionis tick found inside a house in southern Sweden in 2019 was collected. Ticks were screened for Borrelia spp. using a genus-specific quantitative PCR assay. The Borrelia species of the positive specimens were determined by conventional PCR followed by DNA sequencing and phylogenetic analyses. A total of 24% (22 of 92) of the analyzed C. vespertilionis ticks were Borrelia-positive. Phylogenetic analyses indicate that the bacteria belong to the relapsing fever group of borreliae; some of them appear to be identical with Borrelia sp. CPB1, a spirochete only found twice before-in the United Kingdom and in France. Our results also indicate a temporal and spatial distribution of this Borrelia species. Since C. vespertilionis occasionally bites humans, and since it exhibits a high prevalence of Borrelia bacteria, it is possible that it presents a risk of human disease. Further studies are needed to characterize Borrelia sp. CPB1 to determine if it is human-pathogenic and to determine if C. vespertilionis is a vector and/or reservoir of this agent.

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  • 20.
    Jaenson, Thomas G. T.
    et al.
    Uppsala Univ, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    First records of tick-borne pathogens in populations of the taiga tick Ixodes persulcatus in Sweden2019In: Parasites & Vectors, E-ISSN 1756-3305, Vol. 12, no 1, article id 559Article in journal (Refereed)
    Abstract [en]

    Background: The common tick Ixodes ricinus and the taiga tick I. persulcatus are the main tick vectors of Borrelia spirochaetes, TBE virus (TBEV) and of several other zoonotic pathogens in the western and eastern areas, respectively of the Palaearctic region. Recently, populations of the taiga tick were, for the first time, detected in northern Sweden. This prompted us to investigate if they harbour human pathogens. Methods: A total of 276 I. persulcatus ticks (136 males, 126 females and 14 nymphs) and one I. ricinus nymph was collected by the cloth-dragging method in northern Sweden in July-August 2015 and May-July 2016. In addition, 8 males and 10 females of I. persulcatus were collected from two dogs (16 and 2 ticks, respectively) in two of the localities. All ticks were microscopically and molecularly identified to developmental stage and species and screened for B. burgdorferi (sensu lato), B. miyamotoi, Anaplasma phagocytophilum, Rickettsia spp., Neoehrlichia mikurensis, Babesia spp. and TBEV using real-time PCR followed by species identification by sequencing the PCR-products of conventional PCR assays. Results: Of the ticks collected by the cloth-dragging method, 55% (152/277) were positive for Borrelia. There was no significant difference between the proportions of Borrelia-infected nymphs (33%, 5/15) and Borrelia-infected adult ticks (56%, 147/262), and no significant difference between the proportions of Borrelia-infected males (54%, 74/136) and Borrelia-infected females (58%, 73/126). Three different Borrelia species were identified. Borrelia afzelii was the predominant species and detected in 46% of all Borrelia-infected ticks followed by B. garinii, 35%, B. valaisiana, 1%, and mixed infections of different Borrelia species, 1%; 17% of all Borrelia-infections were untypeable. One I. persulcatus female contained Rickettsia helvetica, and one nymph contained Rickettsia sp. Of the 277 ticks analysed, all were negative for A. phagocytophilum, Babesia spp., Borrelia miyamotoi, N. mikurensis and TBEV. The ticks collected from the two dogs were negative for all pathogens examined except for Borrelia spp., that was detected in 5 out of 16 ticks removed from one of the dogs. Conclusions: To our knowledge, this is the first time that I. persulcatus from Sweden has been analysed for the presence of tick-borne pathogens. The examined tick populations had a low diversity of tick-borne pathogens but a high prevalence of B. burgdorferi (s.l.).

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  • 21.
    Jonsson Henningsson, Anna
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Asgeirsson, Hilmir
    Karolinska Inst, Sweden; Karolinska Univ Hosp, Sweden.
    Hammas, Berit
    Karolinska Univ Hosp, Sweden.
    Karlsson, Elias
    Danderyd Hosp, Sweden.
    Parke, Asa
    Karolinska Univ Hosp, Sweden.
    Hoornstra, Dieuwertje
    Acad Med Ctr, Netherlands.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Hovius, Joppe W.
    Acad Med Ctr, Netherlands.
    Two Cases of Borrelia miyamotoi Meningitis, Sweden, 20182019In: Emerging Infectious Diseases, ISSN 1080-6040, E-ISSN 1080-6059, Vol. 25, no 10, p. 1965-1968Article in journal (Refereed)
    Abstract [en]

    We report 2 human cases of Borrelia miyamotoi disease diagnosed in Sweden, including 1 case of meningitis in an apparently immunocompetent patient. The diagnoses were confirmed by 3 different independent PCR assays and DNA sequencing from cerebrospinal fluid, supplemented by serologic analyses.

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  • 22.
    Kjaer, Lene Jung
    et al.
    Univ Copenhagen, Denmark.
    Johansson, Magnus
    Orebro Univ, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Lab Med, Sweden.
    Asghar, Naveed
    Orebro Univ, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Lab Med, Sweden.
    Fredlund, Hans
    Orebro Univ, Sweden; Orebro Cty Council, Sweden.
    Christensson, Madeleine
    Swedish Univ Agr Sci SLU, Sweden.
    Wallenhammar, Amelie
    Orebro Univ, Sweden.
    Bodker, Rene
    Univ Copenhagen, Denmark.
    Rasmussen, Gunlog
    Orebro Univ, Sweden; Orebro Cty Council, Sweden.
    Kjellander, Petter
    Swedish Univ Agr Sci SLU, Sweden.
    Potential drivers of human tick-borne encephalitis in the orebro region of Sweden, 2010-20212023In: Scientific Reports, E-ISSN 2045-2322, Vol. 13, no 1Article in journal (Refereed)
    Abstract [en]

    Incidence of tick-borne encephalitis (TBE) has increased during the last years in Scandinavia, but the underlying mechanism is not understood. TBE human case data reported between 2010 and 2021 were aggregated into postal codes within orebro County, south-central Sweden, along with tick abundance and environmental data to analyse spatial patterns and identify drivers of TBE. We identified a substantial and continuing increase of TBE incidence in orebro County during the study period. Spatial cluster analyses showed significant hotspots (higher number of cases than expected) in the southern and northern parts of orebro County, whereas a cold spot (lower number of cases than expected) was found in the central part comprising orebro municipality. Generalised linear models showed that the risk of acquiring TBE increased by 12.5% and 72.3% for every percent increase in relative humidity and proportion of wetland forest, respectively, whereas the risk decreased by 52.8% for every degree Celsius increase in annual temperature range. However, models had relatively low goodness of fit (R-2 &lt; 0.27). Results suggest that TBE in orebro County is spatially clustered, however variables used in this study, i.e., climatic variables, forest cover, water, tick abundance, sheep as indicator species, alone do not explain this pattern.

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  • 23.
    Labbe Sandelin, Lisa
    et al.
    Uppsala University, Sweden; Kalmar County Hospital, Sweden.
    Tolf, Conny
    Linnaeus University, Sweden.
    Larsson, Sara
    Linnaeus University, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Salaneck, Erik
    Uppsala University, Sweden.
    Jaenson, Thomas G. T.
    Uppsala University, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Olsen, Bjorn
    Uppsala University, Sweden.
    Waldenstrom, Jonas
    Linnaeus University, Sweden.
    Candidatus Neoehrlichia mikurensis in Ticks from Migrating Birds in Sweden2015In: PLOS ONE, E-ISSN 1932-6203, Vol. 10, no 7, p. e0133250-Article in journal (Refereed)
    Abstract [en]

    Candidatus Neoehrlichia mikurensis (CNM; family Anaplasmataceae) was recently recognized as a potential tick-borne human pathogen. The presence of CNM in mammals, in host-seeking Ixodes ticks and in ticks attached to mammals and birds has been reported recently. We investigated the presence of CNM in ornithophagous ticks from migrating birds. A total of 1,150 ticks (582 nymphs, 548 larvae, 18 undetermined ticks and two adult females) collected from 5,365 birds captured in south-eastern Sweden was screened for CNM by molecular methods. The birds represented 65 different species, of which 35 species were infested with one or more ticks. Based on a combination of morphological and molecular species identification, the majority of the ticks were identified as Ixodes ricinus. Samples were initially screened by real-time PCR targeting the CNM 16S rRNA gene, and confirmed by a second real-time PCR targeting the groEL gene. For positive samples, a 1260 base pair fragment of the 16S rRNA gene was sequenced. Based upon bacterial gene sequence identification, 2.1% (24/1150) of the analysed samples were CNM-positive. Twenty-two out of 24 CNM-positive ticks were molecularly identified as I. ricinus nymphs, and the remaining two were identified as I. ricinus based on morphology. The overall CNM prevalence in I. ricinus nymphs was 4.2%. None of the 548 tested larvae was positive. CNM-positive ticks were collected from 10 different bird species. The highest CNM-prevalences were recorded in nymphs collected from common redpoll (Carduelis flammea, 3/7), thrush nightingale (Luscinia luscinia, 2/29) and dunnock (Prunella modularis, 1/17). The 16S rRNA sequences obtained in this study were all identical to each other and to three previously reported European strains, two of which were obtained from humans. It is concluded that ornithophagous ticks may be infected with CNM and that birds most likely can disperse CNM-infected ticks over large geographical areas.

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  • 24.
    Lager, Malin
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences.
    Dessau, Ram B.
    Department of Clinical Microbiology, Slagelse Hospital, Slagelse, Denmark.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences.
    Nyman, Dag
    The Åland Group for Borrelia Research, Åland, Mariehamn, Finland.
    Jensen, Guro F.
    Department of Medical Microbiology, Sørlandet Hospital, Kristiansand, Norway.
    Matussek, Andreas
    Linköping University, Department of Clinical and Experimental Medicine. Linköping University, Faculty of Medicine and Health Sciences. Division of Clinical Microbiology, Laboratory Medicine, Jönköping Region Jönköping County, Sweden, Ryhov County Hospital, Jönköping, Sweden; Karolinska University Laboratory, Stockholm, Sweden; Division of Clinical Microbiology, Department of Laboratory Medicine, Karolinska Institutet, Karolinska University Hospital Huddinge, Stockholm, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Division of Clinical Microbiology, Laboratory Medicine, Jönköping Region Jönköping County, Sweden.
    Jonsson Henningsson, Anna
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Division of Clinical Microbiology, Laboratory Medicine, Jönköping Region Jönköping County, Sweden.
    Serrander, Lena (Contributor)
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology, Infection and Inflammation. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Center for Diagnostics, Department of Clinical Microbiology.
    Serological diagnostics of Lyme borreliosis: comparison of assays in twelve clinical laboratories in Northern Europe2019In: European Journal of Clinical Microbiology and Infectious Diseases, ISSN 0934-9723, E-ISSN 1435-4373, Vol. 38, no 10, p. 1933-1945Article in journal (Refereed)
    Abstract [en]

    Lyme borreliosis (LB), caused by spirochetes belonging to the Borrelia burgdorferi sensu lato complex, is the most common tick-borne infection in Europe. Laboratory diagnosis of LB is mainly based on the patients’ medical history, clinical signs and symptoms in combination with detection of Borrelia-specific antibodies where indirect enzyme-linked-immunosorbent assay (ELISA) is the most widely used technique. The objective of the study was to evaluate and compare the diagnostic accuracy (sensitivities and specificities) of serological tests that are currently in use for diagnosis of LB in clinical laboratories in Northern Europe, by use of a large serum panel. The panel consisted of 195 serum samples from well-characterized and classified patients under investigation for clinically suspected LB (n = 59) including patients with Lyme neuroborreliosis, Lyme arthritis, acrodermatitis chronica atrophicans, erythema migrans or other diseases (n = 112). A total of 201 serum samples from healthy blood donors were also included. The panel (396 serum samples altogether) was sent to 12 clinical laboratories (using five different ELISA methods) as blinded for group affiliation and the laboratories were asked to perform serological analysis according to their routine procedure. The results from the study demonstrated high diagnostic concordance between the laboratories using the same diagnostic assay and lower diagnostic concordance between laboratories using different diagnostic assays. For IgG, the results were in general rather homogenous and showed an average sensitivity of 88% (range 85–91%) compared to IgM which showed lower average sensitivity of 59% (range 50–67%) and more heterogeneous results between assays and laboratories. © 2019, The Author(s).

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  • 25.
    Lager, Malin
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Regional Jonköping County, Sweden.
    Faller, Maximilian
    German National Reference Centre Borrelia, Germany.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Regional Jonköping County, Sweden.
    Kjelland, Vivian
    University of Agder, Norway; Hospital Southern Norway Trust, Norway.
    Andreassen, Ashild
    Norwegian Institute Public Heatlh, Norway.
    Dargis, Rimtas
    Slagelse Hospital, Denmark.
    Quarsten, Hanne
    Hospital Southern Norway Trust, Norway.
    Dessau, Ram
    Slagelse Hospital, Denmark.
    Fingerle, Volker
    German National Reference Centre Borrelia, Germany.
    Margos, Gabriele
    German National Reference Centre Borrelia, Germany.
    Noraas, Solvi
    Hospital Southern Norway Trust, Norway.
    Ornstein, Katharina
    Skånevard Kryh, Sweden.
    Petersson, Ann-Cathrine
    Department Clin Microbiol, Sweden.
    Matussek, Andreas
    Regional Jonköping County, Sweden; Karolinska University of Lab, Sweden; Karolinska Institute, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Regional Jonköping County, Sweden.
    Henningsson, Anna
    Regional Jonköping County, Sweden.
    Molecular detection of Borrelia burgdorferi sensu lato - An analytical comparison of real-time PCR protocols from five different Scandinavian laboratories2017In: PLOS ONE, E-ISSN 1932-6203, Vol. 12, no 9, article id e0185434Article in journal (Refereed)
    Abstract [en]

    Introduction Lyme borreliosis (LB) is the most common tick transmitted disease in Europe. The diagnosis of LB today is based on the patient A s medical history, clinical presentation and laboratory findings. The laboratory diagnostics are mainly based on antibody detection, but in certain conditions molecular detection by polymerase chain reaction (PCR) may serve as a complement. Aim The purpose of this study was to evaluate the analytical sensitivity, analytical specificity and concordance of eight different real-time PCR methods at five laboratories in Sweden, Norway and Denmark. Method Each participating laboratory was asked to analyse three different sets of samples (reference panels; all blinded) i) cDNA extracted and transcribed from water spiked with cultured Borrelia strains, ii) cerebrospinal fluid spiked with cultured Borrelia strains, and iii) DNA dilution series extracted from cultured Borrelia and relapsing fever strains. The results and the method descriptions of each laboratory were systematically evaluated. Results and conclusions The analytical sensitivities and the concordance between the eight protocols were in general high. The concordance was especially high between the protocols using 16S rRNA as the target gene, however, this concordance was mainly related to cDNA as the type of template. When comparing cDNA and DNA as the type of template the analytical sensitivity was in general higher for the protocols using DNA as template regardless of the use of target gene. The analytical specificity for all eight protocols was high. However, some protocols were not able to detect Borrelia spielmanii, Borrelia lusitaniae or Borrelia japonica.

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  • 26.
    Lager, Malin
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    Matussek, Andreas
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Oslo Univ Hosp, Norway; Univ Oslo, Norway.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    Jonsson Henningsson, Anna
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Center for Diagnostics, Department of Clinical Microbiology.
    Molecular Detection of Borrelia Bacteria in Cerebrospinal Fluid-Optimisation of Pre-Analytical Sample Handling for Increased Analytical Sensitivity2021In: Diagnostics, ISSN 2075-4418, Vol. 11, no 11, article id 2088Article in journal (Refereed)
    Abstract [en]

    The main tools for clinical diagnostics of Lyme neuroborreliosis (LNB) are based on serology, i.e., detection of antibodies in cerebrospinal fluid (CSF). In some cases, PCR may be used as a supplement, e.g., on CSF from patients with early LNB. Standardisation of the molecular methods and systematic evaluation of the pre-analytical handling is lacking. To increase the analytical sensitivity for detection of Borrelia bacteria in CSF by PCR targeting the 16S rRNA gene, parameters were systematically evaluated on CSF samples spiked with a known amount of cultured Borrelia bacteria. The results showed that the parameters such as centrifugation time and speed, the use of complementary DNA as a template (in combination with primers and a probe aiming at target gene 16S rRNA), and the absence of inhibitors (e.g., erythrocytes) had the highest impact on the analytical sensitivity. Based on these results, a protocol for optimised handling of CSF samples before molecular analysis was proposed. However, no clinical evaluation of the proposed protocol has been done so far, and further investigations of the diagnostic sensitivity need to be performed on well-characterised clinical samples from patients with LNB.

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  • 27.
    Larsson, Clarinda
    et al.
    Linköping University, Faculty of Medicine and Health Sciences.
    Hvidsten, Dag
    Univ Hosp North Norway, Norway; Nordland Hosp, Norway.
    Stuen, Snorre
    Norwegian Univ Life Sci, Norway.
    Jonsson Henningsson, Anna
    Linköping University, Department of Clinical and Experimental Medicine, Division of Neuro and Inflammation Science. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Candidatus Neoehrlichia mikurensis” in Ixodes ricinus ticks collected near the Arctic Circle in Norway2018In: Parasites & Vectors, E-ISSN 1756-3305, Vol. 11, article id 620Article in journal (Refereed)
    Abstract [en]

    Background: "Candidatus Neoehrlichia mikurensis" is a gram-negative bacterium belonging to the family Anaplasmataceae that, in Europe, is transmitted by Ixodes ricinus ticks. Candidatus N. mikurensis can cause a severe systemic inflammatory syndrome, neoehrlichiosis, mostly in persons with other underlying diseases. To date, "Ca. N. mikurensis "has been found in ticks in different countries in Asia and Europe, but never as far north as at the Arctic Circle. Methods: A total of 1104 I. ricinus ticks collected from vegetation and from animals in northern Norway (64-68 degrees N) were analysed for the prevalence of "Ca. N. mikurensis". Of them, 495 ticks were collected from vegetation by flagging and 609 ticks were collected from dogs and cats. Total nucleic acid extracted from the ticks were converted to cDNA and analyzed with real-time PCR targeting the 16S rRNA gene of "Ca. N. mikurensis". Positive samples were further analysed by nested PCR and sequencing. Results: "Candidatus N. mikurensis" was detected in 11.2% of all collected I. ricinus ticks in northern Norway. The prevalence differed between ticks collected from vegetation (18.2%; 90/495) compared to ticks collected from dogs and cats (5.6%; 34/609). The ticks from dogs and cats were collected in Bronnoy area and seven additional districts further north. The prevalence of "Ca. N. mikurensis" in these ticks differed between geographical localities, with the highest prevalence in the Bronnoy area. Conclusions: The detection of "Ca. N. mikurensis" in I. ricinus ticks from the Arctic Circle in northern Norway indicates potential risk for tick-bitten humans at this latitude to be infected with "Ca. N. mikurensis".

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  • 28.
    Lindblom, Anders
    et al.
    Uppsala University, Sweden; Clin Research Centre, Sweden.
    Wallmenius, Katarina
    Uppsala University, Sweden.
    Sjöwall, Johanna
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Heart and Medicine Center, Department of Infectious Diseases.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine, Division of Neuro and Inflammation Science. Linköping University, Faculty of Medicine and Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. County Hospital Ryhov, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. County Hospital Ryhov, Sweden.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Heart and Medicine Center, Department of Infectious Diseases.
    Nilsson, Kenneth
    Uppsala University, Sweden; Clin Research Centre, Sweden.
    Prevalence of Rickettsia spp. in Ticks and Serological and Clinical Outcomes in Tick-Bitten Individuals in Sweden and on the Aland Island2016In: PLOS ONE, E-ISSN 1932-6203, Vol. 11, no 11, article id e0166653Article in journal (Refereed)
    Abstract [en]

    Tick-transmitted diseases are an emerging health problem, and the hard tick Ixodes ricinus is the main vector for Borrelia spp., tick-borne encephalitis virus and most of the spotted fever Rickettsiae in Europe. The aim of the present study was to examine the incidence of rickettsial infection in the southernmost and south central parts of Sweden and the Aland Islands in Finland the risk of infection in humans and its correlation with a bite of a Rickettsia-infected tick, the self-reported symptoms of rickettsial disease, and the prevalence of co-infection between Rickettsia spp. and Borrelia spp. Persons with a recent tick bite were enrolled through public media and asked to answer a questionnaire, provide a blood sample and bring detached ticks at enlistment and at follow-up three months later. Blood samples were previously analysed for Borrelia spp. antibodies and, for this report, analysed for antibodies to Rickettsia spp. by immunofluorescence and in 16 cases also using Western Blot. Ninety-six (44.0%) of the 218 participants were seropositive for IgG antibodies to Rickettsia spp. Forty (18.3%) of the seropositive participants had increased titres at the follow-up, indicating recent/current infection, while four (1.8%) had titres indicating probable recent/current infection (amp;gt;= 1: 256). Of 472 ticks, 39 (8.3%) were Rickettsia sp. positive. Five (31.3%) of 16 participants bitten by a Rickettsia-infected tick seroconverted. Experience of the selfreported symptoms nausea (p = 0.006) and radiating pain (p = 0.041) was more common among those with recent, current or probable infection compared to those who did not seroconvert. Participants who showed seroreactivity or seroconversion to Rickettsia spp. had more symptoms than those who were seronegative. Seven (3.2%) participants showed seroconversion to Borrelia spp., and three (1.4%) of these showed seroconversion to both Rickettsia spp. and Borrelia spp., in accordance with previous studies in Sweden. Symptoms of rickettsial disease were in most of the cases vague and general that were difficult to differentiate from other tick-borne diseases.

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  • 29.
    Lindblom, Pontus
    et al.
    Linköping University, Faculty of Health Sciences. Linköping University, Department of Clinical and Experimental Medicine.
    Wilhelmsson, Peter
    Linköping University, Faculty of Health Sciences. Linköping University, Department of Clinical and Experimental Medicine.
    Fryland, Linda
    Linköping University, Faculty of Health Sciences. Linköping University, Department of Clinical and Experimental Medicine.
    Matussek, Andreas
    County Hospital Ryhov, Jönköping.
    Haglund, Mats
    Kalmar County hospital.
    Sjöwall, Johanna
    Linköping University, Faculty of Health Sciences. Linköping University, Department of Clinical and Experimental Medicine. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Vene, Sirkka
    Swedish Institute for Communicable Disease Control, Stockholm.
    Nyman, Dag
    Åland Central Hospital, Åland, Finland.
    Forsberg, Pia
    Linköping University, Faculty of Health Sciences. Linköping University, Department of Clinical and Experimental Medicine. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Faculty of Health Sciences. Linköping University, Department of Clinical and Experimental Medicine.
    Determining factors for successful vaccination against tick-borne encephalitis virus in older individuals2014Manuscript (preprint) (Other academic)
    Abstract [en]

    We performed a cross-sectional study including 533 persons (median age 61) from the highly TBE endemic Åland Islands in the archipelago between Sweden and Finland. Blood samples, questionnaires and vaccination records were obtained from all study participants. The aim was to investigate if there was any association between TBEV antibody titer and 14 healthrelated factors: [age, gender, number of vaccine doses (0-5), time since last vaccine dose, previous TBE disease, vaccination against other flaviviruses, ≥2 tick-bites during the previous 3 months, pet-ownership, asthma, smoking, allergy, diabetes, medication, and previous tumor]. Measurement of TBEV IgG antibodies was performed using two commercial ELISA assays (Enzygnost and Immunozym), and a third in-house rapid fluorescent focus inhibition test was used to measure TBEV neutralizing antibodies. The age of the person and the number of vaccine doses were the two most important factors determining successful vaccination. The response to each vaccine dose declined linearly with increased age. A 35 year age difference corresponds to a vaccine dose increment from 3 to 4 to achieve the same response. Participants receiving medication and participants previously vaccinated against other flaviviruses had lower TBEV antibody titers on average, while those with self-reported asthma had higher titers. By comparing the 3 serological assays we show that the Enzygnost and Immunozym assay differ due to choice of cutoffs, but not in overall accuracy.

  • 30.
    Lindblom, Pontus
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Matussek, Andreas
    County Hospital Ryhov, Sweden .
    Haglund, Mats
    County Hospital Kalmar, Sweden .
    Sjöwall, Johanna
    Linköping University, Department of Clinical and Experimental Medicine, Division of Clinical Sciences. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Vene, Sirkka
    Public Health Agency Sweden, Stockholm.
    Nyman, Dag
    Aland Central Hospital, Finland .
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Factors Determining Immunological Response to Vaccination against Tick-Borne Encephalitis Virus in Older Individuals2014In: PLOS ONE, E-ISSN 1932-6203, Vol. 9, no 6, p. e0100860-Article in journal (Refereed)
    Abstract [en]

    We performed a cross-sectional study including 533 individuals (median age 61) from the highly TBE endemic A land Islands in the archipelago between Sweden and Finland. Blood samples, questionnaires and vaccination records were obtained from all study participants. The aim was to investigate if there was any association between TBEV antibody titer and 12 health-related factors. Measurement of TBEV IgG antibodies was performed using two commercial ELISA assays (Enzygnost and Immunozym), and a third in-house rapid fluorescent focus inhibition test was used to measure TBEV neutralizing antibodies. The age of the individual and the number of vaccine doses were the two most important factors determining the immunological response to vaccination. The response to each vaccine dose declined linearly with increased age. A 35 year age difference corresponds to a vaccine dose increment from 3 to 4 to achieve the same immunological response. Participants previously vaccinated against other flaviviruses had lower odds of being seropositive for neutralizing TBEV antibodies on average, while participants with self-reported asthma had higher odds of being seropositive. By comparing the 3 serological assays we show that the Enzygnost and Immunozym assay differ due to choice of cutoffs, but not in overall accuracy.

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  • 31.
    Lindblom, Pontus
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine, Division of Inflammation Medicine. Linköping University, Faculty of Health Sciences.
    Sjowall, Johanna
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Haglund, Mats
    Kalmar County hospital.
    Matussek, Andreas
    County Hospital Ryhov, Jönköping.
    Ernerudh, Jan
    Linköping University, Department of Clinical and Experimental Medicine, Clinical Immunology. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Center for Diagnostics, Department of Clinical Immunology and Transfusion Medicine.
    Vene, Sirkka
    Swedish Institute for Communicable Disease Control, Stockholm.
    Nyman, Dag
    Åland Central Hospital, Åland, Finland.
    Andreassen, Åshild
    Norwegian Institute of Public Health, Olso, Norway.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Tick-borne encephalitis virus in ticks detached from humans and follow-up of serological and clinical response.2014In: Ticks and Tick Borne Diseases, ISSN 1877-959X, Vol. 5, no 1, p. 21-28Article in journal (Refereed)
    Abstract [en]

    The risk of tick-borne encephalitis virus (TBEV) infection after a tick bite remains largely unknown. To address this, we investigated the presence of TBEV in ticks detached from humans in an attempt to relate viral copy number, TBEV subtype, and tick feeding time with the serological and clinical response of the tick-bitten participants. Ticks, blood samples, and questionnaires were collected from tick-bitten humans at 34 primary health care centers in Sweden and in the Aland Islands (Finland). A total of 2167 ticks was received from 1886 persons in 2008-2009. Using a multiplex quantitative real-time PCR, 5 TBEV-infected ticks were found (overall prevalence 0.23%, copy range <4 X 10(2)-7.7 X 10(6) per tick). One unvaccinated person bitten by a tick containing 7.7 x 10(6) TBEV copies experienced symptoms. Another unvaccinated person bitten by a tick containing 1.8 x 10(3) TBEV copies developed neither symptoms nor TBEV antibodies. The remaining 3 persons were protected by vaccination. In contrast, despite lack of TBEV in the detached ticks, 2 persons developed antibodies against TBEV, one of whom reported symptoms. Overall, a low risk of TBEV infection was observed, and too few persons got bitten by TBEV-infected ticks to draw certain conclusions regarding the clinical outcome in relation to the duration of the blood meal and virus copy number. However, this study indicates that an antibody response may develop without clinical symptoms, that a bite by an infected tick not always leads to an antibody response or clinical symptoms, and a possible correlation between virus load and tick feeding time. (C) 2013 Elsevier GmbH. All rights reserved.

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  • 32.
    Ocias, Lukas Frans
    et al.
    Statens Serum Inst, Denmark; Rigshosp, Denmark.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Sjöwall, Johanna
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Medicine Center, Department of Infectious Diseases.
    Henningsson, Anna J.
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Center for Diagnostics, Department of Clinical Microbiology. Division of Clinical Microbiology, Laboratory Medicine, Jönköping Region Jönköping County, Sweden.
    Nordberg, Marika
    Aland Cent Hosp, Finland.
    Jorgensen, Charlotte Svaerke
    Statens Serum Inst, Denmark.
    Krogfelt, Karen Angeliki
    Statens Serum Inst, Denmark; Roskilde Univ, Denmark.
    Forsberg, Pia
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Cty Hosp Ryhov, Sweden.
    Emerging tick-borne pathogens in the Nordic countries: A clinical and laboratory follow-up study of high-risk tick-bitten individuals2020In: Ticks and Tick-borne Diseases, ISSN 1877-959X, E-ISSN 1877-9603, Vol. 11, no 1, article id UNSP 101303Article in journal (Refereed)
    Abstract [en]

    Despite the presence of several microorganisms, other than Borrelia burgdorferi sensu lato (Bbsl) and TBE virus, in Ixodes ricinus ticks from the Nordic countries, data is lacking on their pathogenic potential in humans. In this study, we wanted to investigate the aetiology and clinical manifestations of tick-transmitted infections in individuals seeking medical care following a tick-bite. The sampling frame was participants of a large-scale, prospective, multi-centre, follow-up study of tick-bitten volunteers recruited in Sweden, Finland and Norway in the years 2007-2015. Participants who sought medical care during the three-month follow-up period and from whom blood samples were collected during this healthcare visit (n=92) were tested, using PCR, for exposure to spotted fever group (SFG) Rickettsia spp., Anaplasma phagocytophilum and Babesia spp. Moreover, 86 of these individuals had two serum samples, collected three months apart, tested serologically for six tick-borne microorganisms. The selected organisms-Bbsl, SFG rickettsiae, Anaplasma phagocytophilum, TBE virus, Babesia microti and Bartonella henselae-have all been detected in field-collected ticks from the Nordic countries. Medical records were reviewed and questionnaires were completed to determine clinical manifestations. We found Lyme borreliosis to be the most common tick-transmitted infection as seen in 46 (54%) of the 86 participants with available medical records. Among the 86 participants with paired sera, serological or molecular evidence of recent exposure to other microorganisms than Bbsl could be demonstrated in eight (9%). Five participants (6%) exhibited serological evidence of recent concomitant exposure to more than one tick-borne microorganism. Clinical presentations were mild with one exception (TBE). In conclusion, our data suggest a low risk of infection with tick-borne microorganisms, other than Bbsl, in immunocompetent tick-bitten persons from the examined regions, a low occurrence of co-infection and mostly mild or no overt clinical signs of infection in immunocompetent persons exposed to the studied agents.

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  • 33.
    Ortiz-Baez, Ayda Susana
    et al.
    Univ Sydney, Australia.
    Jaenson, Thomas G. T.
    Uppsala Univ, Sweden.
    Holmes, Edward C.
    Univ Sydney, Australia.
    Pettersson, John H. -O.
    Univ Sydney, Australia; Uppsala Univ, Sweden; Uppsala Univ Hosp, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Substantial viral and bacterial diversity at the bat-tick interface2023In: Microbial Genomics, E-ISSN 2057-5858, Vol. 9, no 3, article id 000942Article in journal (Refereed)
    Abstract [en]

    Ticks harbour a high diversity of viruses, bacteria and protozoa. The soft tick Carios vespertilionis (Argasidae) is a common ectoparasite of bats in the Palearctic region and is suspected to be vector and reservoir of viruses and other microbial species in bat populations, some of which may act as zoonotic agents for human disease. The Soprano pipistrelle (Pipistrellus pygmaeus, Vespertilionidae) is widely distributed in Europe, where it can be found inside or close to human habitation. We used metatranscriptomic sequencing to determine the RNA virome and common microbiota in blood- fed C. vespertilionis ticks collected from a Soprano pipistrelle bat roosting site in south- central Sweden. Our analyses identified 16 viruses from 11 virus families, of which 15 viruses were novel. For the first time in Sweden we identified Issuk- Kul virus, a zoonotic arthropod- borne virus previously associated with outbreaks of acute febrile illness in humans. Probable bat- associated and tick- borne viruses were classified within the families Nairoviridae, Caliciviridae and Hepeviridae, while other invertebrate- associated viruses included members of the Dicistroviridae, Iflaviridae, Nodaviridae, Partitiviridae, Permutotetraviridae, Polycipiviridae and Solemoviridae. Similarly, we found abundant bacteria in C. vespertilionis, including genera with known tick- borne bacteria, such as Coxiella spp. and Rickettsia spp. These findings demonstrate the remarkable diversity of RNA viruses and bacteria present in C. vespertilionis and highlight the importance of bat- associated ectoparasite surveillance as an effective and non- invasive means to track viruses and bacteria circulating in bats and ticks.

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  • 34.
    Pawelczyk, Olga
    et al.
    Med Univ Siles, Poland.
    Kotela, Damian
    Vet Clin Small Anim DAWET, Poland.
    Asman, Marek
    Med Univ Siles, Poland; Med Univ Siles, Poland.
    Witecka, Joanna
    Med Univ Siles, Poland.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Bubel, Paulina
    Vet Clin Small Anim DAWET, Poland.
    Solarz, Krzysztof
    Med Univ Siles, Poland.
    The First Records of Canine Babesiosis in Dogs from Dermacentor reticulatus-Free Zone in Poland2022In: Pathogens, E-ISSN 2076-0817, Vol. 11, no 11, article id 1329Article in journal (Refereed)
    Abstract [en]

    Tick-borne microorganisms belong to important etiological agents of many infectious diseases affecting humans and animals. Among them, there are haemoprotozoans of the Babesia genus, which infect erythrocytes of a host and may cause many clinical symptoms. Canine babesiosis is an emerging tick-borne disease in Southern and Central Europe. In this study, we report two cases of symptomatic canine babesiosis caused by Babesia canis in domestic dogs from the Silesian Voivodeship, Poland, as well as the presence of Dermacentor reticulatus ticks detected on one of the Babesia-infected dogs (D. reticulatus-free zone). The molecular analysis confirmed the presence of Babesia canis in the dogs blood, and the sequencing analysis showed that the obtained sequence is 100% identical to the sequence of Babesia canis isolate 3469 (sequence ID: KX712122.1). Our findings should raise awareness of B. canis infection among dog owners and veterinarians in the region where B. canis was not previously reported in residential, non-traveling dogs, as well as ensuring that adequate diagnostic methods are available.

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  • 35.
    Skogman, Barbro H.
    et al.
    Uppsala Univ, Sweden; Orebro Univ, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Atallah, Stephanie
    Sahlgrens Univ Hosp, Sweden.
    Petersson, Ann-Cathrine
    Clin Microbiol Lab, Sweden.
    Ornstein, Katarina
    Ystad Hosp, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Ryhov Cty Hosp, Sweden.
    Lyme neuroborreliosis in Swedish children-PCR as a complementary diagnostic method for detection of Borrelia burgdorferi sensu lato in cerebrospinal fluid2021In: European Journal of Clinical Microbiology and Infectious Diseases, ISSN 0934-9723, E-ISSN 1435-4373, Vol. 40, no 5, p. 1003-1012Article in journal (Refereed)
    Abstract [en]

    The aim of this study was to evaluate polymerase chain reaction (PCR) as a diagnostic method for the detection of Borrelia burgdorferi s.l. in CSF of Swedish children with LNB. This study was performed retrospectively on CSF and serum samples collected from children evaluated for LNB (n = 233) and controls with other specific neurological disorders (n = 59) in a Swedish Lyme endemic area. For anti-Borrelia antibody index, the IDEIA Lyme Neuroborreliosis kit (Oxoid) was used. Two in-house real-time PCR assays targeting the 16S rRNA gene were evaluated (TaqMan (R) and LUX (TM)). Among patients classified as LNB cases (n = 102), five children (5%) were Borrelia PCR-positive in CSF with the TaqMan (R) assay. In the Non-LNB group (n = 131), one patient was Borrelia PCR positive with the TaqMan (R) assay. Among controls (n = 59), all CSF samples were PCR negative. When amplifying and sequencing ospA, we found B. garinii (n = 2), B. afzelii (n = 2), B. bavariensis (n = 1), and one untypable (n = 1). With the LUX (TM) technology, all CSF samples were PCR negative. The TaqMan (R) assay could detect only few cases (n = 6) of B. burgdorferi s.l. in CSF among children with LNB and the sensitivity was very low (5%). However, using larger CSF volumes and centrifugation of samples, the PCR technique could still be useful as a complementary diagnostic method when evaluating LNB. Furthermore, detection of spirochete DNA in clinical matrices, including CSF, is the method of choice for studying epidemiological aspects of LNB, a tick-borne emerging disease.

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  • 36.
    Tompa, Eszter
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    Jaenson, Thomas G. T.
    Uppsala Univ, Sweden.
    Wilhelmsson, Peter
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Sweden.
    First Records of Possibly Human Pathogenic Rickettsia Species in Bat Ticks, Carios vespertilionis, in Sweden2023In: Microorganisms, E-ISSN 2076-2607, Vol. 11, no 2, article id 357Article in journal (Refereed)
    Abstract [en]

    The Soprano pipistrelle bat, Pipistrellus pygmaeus, is a common species in large parts of Sweden. Many of its natural habitats are near human habitations. This creates opportunities for ticks infesting these bats to encounter humans and possibly transmit zoonotic pathogens by tick bites. The bats are often infested with Carios vespertilionis, a tick species that, in addition to bats, has been recorded to bite humans on occasion. This study aimed to investigate if C. vespertilionis acts as a reservoir for Anaplasma phagocytophilum, Neoehrlichia mikurensis, Tick-borne encephalitis virus, and species of Babesia and Rickettsia and to improve currently used conventional PCR protocols for molecular species determination of Rickettsia spp. Ninety-two C. vespertilionis ticks were collected from underneath a bat-box harbouring P. pygmaeus. Pathogen-specific PCR assays showed that 58.4% were positive for Rickettsia spp. and negative for the other pathogens analysed. Phylogenetic analyses indicate that the species belong to R. parkeri, R. conorii, R. slovaca, R. sibirica subsp. mongolotimonae, R. rickettsii, and a hitherto uncultured Rickettsia sp. Several of these species are considered pathogenic to humans. Given the ecology and behaviour of C. vespertilionis, it may be a vector of these rickettsiae among bats and occasionally humans. To determine the Rickettsia species with certainty, and to determine if C. vespertilionis may be a reservoir and vector of the Rickettsia spp., further studies are needed.

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  • 37. Order onlineBuy this publication >>
    Wilhelmsson, Peter
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    A STING from a Tick: Epidemiology, Ecology and Clinical Aspects of Lyme Borreliosis2014Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Lyme borreliosis (LB) is the most common tick-borne disease in the Northern Hemisphere and the number of LB cases is increasing. The infection is caused by spirochetes belonging to the Borrelia burgdorferi sensu lato complex, and is, in Europe, transmitted to humans by Ixodes ricinus ticks.

    To gain a deeper knowledge of the interactions between ticks, humans and Borrelia bacteria, we investigated temporal differences in exposure to tick bites in different parts of Sweden and the Åland Islands, Finland during the years 2008 and 2009. We also investigated the site of tick attachment on the human body and the time it takes for a person to detected and remove such ticks. Furthermore, the distribution of Borrelia species and the number of Borrelia cells in the ticks were investigated. Sera taken from the tick-bitten persons at study inclusion were analyzed for the presence of Borrelia antibodies. Three months later, the clinical outcome and the serological response of the tick-bitten persons were investigated. A total of 2154 I. ricinus ticks and 1546 participants were included in the studies.

    Participants were exposed to tick bites between April and November, but temporal and spatial differences in exposure to ticks was found. The majority of the tick bites were caused by nymphs (70%) and most tick bites took place on the legs (50%). The site of tick attachment on the body as well as the age and gender of the participant influenced how soon a tick was detected. The majority of participants removed “their” ticks later than 24 hours of attachment. Of all ticks, 26% was Borrelia-infected, but the prevalence varied between the life stages of the tick and between the studied areas. Six species of the B. burgdorferi sensu lato complex and one Borrelia species that may cause tick-borne relapsing fever were detected. Adult ticks that had fed more than 36 hours contained a lower number of Borrelia cells than adult ticks that had fed less than 36 hours. The seroprevalence among the participants varied between genders as well as between the studied areas. Of all participants, 2% was diagnosed with LB and 2.5% seroconverted without an LB diagnose. A correlation between seroconversion and duration time of tick attachment was found, but the number of Borrelia cells in the tick, did not explain the risk of infection for the bitten person.

    A deeper knowledge and a better understanding of the interactions between ticks, humans and Borrelia bacteria may contribute reducing the risk for tick bites and the risk of developing LB after a tick bite.

    List of papers
    1. Ixodes ricinus ticks removed from humans in Northern Europe: seasonal pattern of infestation, attachment sites and duration of feeding
    Open this publication in new window or tab >>Ixodes ricinus ticks removed from humans in Northern Europe: seasonal pattern of infestation, attachment sites and duration of feeding
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    2013 (English)In: Parasites & Vectors, E-ISSN 1756-3305, Vol. 6, no 362Article in journal (Refereed) Published
    Abstract [en]

    BACKGROUND:

    The common tick Ixodes ricinus is the main vector in Europe of the tick-borne encephalitis virus and of several species of the Borrelia burgdorferi sensu lato complex, which are the etiological agents of Lyme borreliosis. The risk to contract bites of I. ricinus is dependent on many factors including the behaviour of both ticks and people. The tick's site of attachment on the human body and the duration of tick attachment may be of clinical importance. Data on I. ricinus ticks, which were found attached to the skin of people, were analysed regarding potentially stage-specific differences in location of attachment sites, duration of tick attachment (= feeding duration), seasonal and geographical distribution of tick infestation in relation to age and gender of the tick-infested hosts.

    METHODS:

    During 2008-2009, 1770 tick-bitten persons from Sweden and the Åland Islands removed 2110 I. ricinus ticks. Participants provided information about the date of tick detection and location on their body of each attached tick. Ticks were identified to species and developmental stage. The feeding duration of each nymph and adult female tick was microscopically estimated based on the scutal and the coxal index.

    RESULTS:

    In 2008, participants were tick-bitten from mid-May to mid-October and in 2009 from early April to early November. The infestation pattern of the nymphs was bimodal whereas that of the adult female ticks was unimodal with a peak in late summer. Tick attachment site on the human body was associated with stage of the tick and gender of the human host. Site of attachment seemed to influence the duration of tick feeding. Overall, 63% of nymphs and adult female ticks were detected and removed more than 24 hours after attachment. Older persons, compared to younger ones, and men, compared to women, removed "their" ticks after a longer period of tick attachment.

    CONCLUSIONS:

    The infestation behaviour of the different tick stages concerning where on the host's body the ticks generally will attach and when such ticks generally will be detected and removed in relation to host age and gender, should be of value for the development of prophylactic methods against tick infestation and to provide relevant advice to people on how to avoid or reduce the risk of tick infestation.

    Place, publisher, year, edition, pages
    BioMed Central, 2013
    Keywords
    Ixodes ricinus; Tick infestation; Tick bite; Attachment site; Feeding behaviour; Feeding duration; Host-seeking behaviour; Seasonal activity; Sweden; Åland
    National Category
    Medical and Health Sciences
    Identifiers
    urn:nbn:se:liu:diva-103499 (URN)10.1186/1756-3305-6-362 (DOI)000330064200001 ()24360096 (PubMedID)
    Available from: 2014-01-20 Created: 2014-01-20 Last updated: 2024-01-17Bibliographically approved
    2. Prevalence and Diversity of Borrelia Species in Ticks That Have Bitten Humans in Sweden
    Open this publication in new window or tab >>Prevalence and Diversity of Borrelia Species in Ticks That Have Bitten Humans in Sweden
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    2010 (English)In: JOURNAL OF CLINICAL MICROBIOLOGY, ISSN 0095-1137, Vol. 48, no 11, p. 4169-4176Article in journal (Refereed) Published
    Abstract [en]

    Members of the genus Borrelia are among the most common infectious agents causing tick-borne disease in humans worldwide. Here, we developed a Light Upon eXtension (LUX) real-time PCR assay that can detect and quantify Borrelia species in ticks that have fed on humans, and we applied the assay to 399 such ticks. Borrelia PCR-positive ticks were identified to species level by sequencing the products of conventional PCR performed using Borrelia group-specific primers. There was a 19% prevalence of Borrelia spp. in the detached ticks, and the number of spirochetes per Borrelia PCR-positive tick ranged from 2.0 x 10(2) to 4.9 x 10(5), with a median of 7.8 x 10(3) spirochetes. Adult ticks had a significantly larger number of spirochetes, with a median of 8.4 x 10(4) compared to the median of nymphs of 4.4 x 10(4). Adult ticks also exhibited a higher prevalence of Borrelia (33%) than nymphs (14%). Among the identified species, Borrelia afzelii was found to predominate (61%) and was followed by B. garinii (23%), B. valaisiana (13%), B. burgdorferi sensu stricto (1%), B. lusitaniae (1%), and B. miyamotoi-like (1%). Also, 3% of the ticks were coinfected with multiple strains of B. afzelii. Notably, this is the first report of B. lusitaniae being detected in ticks in Sweden. Our LUX real-time PCR assay proved to be more sensitive than a corresponding TaqMan assay. In conclusion, the novel LUX real-time PCR method is a rapid and sensitive tool for detection and quantification of Borrelia spp. in ticks.

    Place, publisher, year, edition, pages
    American Society for Microbiology, 2010
    National Category
    Medical and Health Sciences
    Identifiers
    urn:nbn:se:liu:diva-62152 (URN)10.1128/JCM.01061-10 (DOI)000283588500049 ()
    Note
    Original Publication: Peter Wilhelmsson, Linda Fryland, Stefan Börjesson, Johan Nordgren, Sven Bergström, Jan Ernerudh, Pia Forsberg and Per-Eric Lindgren, Prevalence and Diversity of Borrelia Species in Ticks That Have Bitten Humans in Sweden, 2010, JOURNAL OF CLINICAL MICROBIOLOGY, (48), 11, 4169-4176. http://dx.doi.org/10.1128/JCM.01061-10 Copyright: American Society for Microbiology http://www.asm.org/ Available from: 2010-11-19 Created: 2010-11-19 Last updated: 2021-12-28
    3. Prevalence, Diversity, and Load of Borrelia species in Ticks That Have Fed on Humans in Regions of Sweden and Åland Islands, Finland with Different Lyme Borreliosis Incidences
    Open this publication in new window or tab >>Prevalence, Diversity, and Load of Borrelia species in Ticks That Have Fed on Humans in Regions of Sweden and Åland Islands, Finland with Different Lyme Borreliosis Incidences
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    2013 (English)In: PLOS ONE, E-ISSN 1932-6203, Vol. 8, no 11, p. e81433-Article in journal (Refereed) Published
    Abstract [en]

    The incidence of Lyme borreliosis (LB) in a region may reflect the prevalence of Borrelia in the tick population. Our aim was to investigate if regions with different LB incidences can be distinguished by studying the prevalence and diversity of Borrelia species in their respective tick populations. The Borrelia load in a feeding tick increases with the duration of feeding, which may facilitate a transmission of Borrelia Spirochetes from tick to host. Therefore, we also wanted to investigate how the Borrelia load in ticks that have fed on humans varies with the duration of tick feeding. During 2008 and 2009, ticks that had bitten humans were collected from four regions of Sweden and Finland, regions with expected differences in LB incidence. The duration of tick feeding was estimated and Borrelia were detected and quantified by a quantitative PCR assay followed by species determination. Out of the 2,154 Ixodes ricinus ticks analyzed, 26% were infected with Borrelia and seven species were identified. B. spielmanii was detected for the first time in the regions. The tick populations collected from the four regions exhibited only minor differences in both prevalence and diversity of Borrelia species, indicating that these variables alone cannot explain the regions different LB incidences. The number of Borrelia cells in the infected ticks ranged from fewer than ten to more than a million. We also found a lower number of Borrelia cells in adult female ticks that had fed for more than 36 hours, compared to the number of Borrelia cells found in adult female ticks that had fed for less than 36 hours.

    Place, publisher, year, edition, pages
    Public Library of Science, 2013
    National Category
    Medical and Health Sciences
    Identifiers
    urn:nbn:se:liu:diva-102779 (URN)10.1371/journal.pone.0081433 (DOI)000327539800130 ()
    Note

    Funding Agencies|Medical Research Council of South-East Sweden|FORSS-8967FORSS-12573FORSS-29021FORSS-86911|Swedish Research Council (Medicine)|2011-345|County Council of Ostergotland||Wilhelm and Else Stockmanns Foundation||Angstromlands Kuturstiftelse||EU Interreg IV A|167226|

    Available from: 2014-01-07 Created: 2013-12-26 Last updated: 2021-06-14
    4. A prospective study on the incidence of Borrelia infection after a tick bite in Sweden and on the Åland Islands, Finland (2008-2009)
    Open this publication in new window or tab >>A prospective study on the incidence of Borrelia infection after a tick bite in Sweden and on the Åland Islands, Finland (2008-2009)
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    2016 (English)In: Ticks and Tick-borne Diseases, ISSN 1877-959X, E-ISSN 1877-9603, Vol. 7, no 1, p. 71-79Article in journal (Refereed) Published
    Abstract [en]

    Lyme borreliosis (LB) is a common and increasing tick-borne disease in Europe. The risk of acquiring a Borrelia infection after a tick bite is not fully known. Therefore, we investigated the incidence of Borrelia infection after a tick bite and if the Borrelia load and/or the duration of tick-feeding influenced the risk of infection. During 2008-2009, ticks and blood samples were collected from 1546 tick-bitten persons from Sweden and the Åland Islands, Finland. Follow-up blood samples were taken three months after the tick bite. The duration of tick feeding was microscopically estimated and Borrelia was detected and quantified in ticks by real-time PCR. Anti-Borrelia antibodies were detected in sera using ELISA assays and immunoblot.

    Even though 28 % of the participants were bitten by a Borrelia-positive tick, only 7.5% (32/428) of them developed a Borrelia infection, half of them LB. All who seroconverted removed “their” ticks significantly later than those who did not. The Borrelia load in the ticks did not explain the risk of seroconversion. Regional as well as gender differences in the Borrelia seroprevalence were found. The risk of developing a Borrelia infection after a bite by a Borrelia-infected tick is small but increases with the duration of tick feeding.

    Place, publisher, year, edition, pages
    Elsevier, 2016
    Keywords
    Borrelia burgdorferi sensu lato; tick bite; incidence of infection; Lyme borreliosis; asymptomatic infection; bacterial load; tick-feeding.
    National Category
    Infectious Medicine
    Identifiers
    urn:nbn:se:liu:diva-105475 (URN)10.1016/j.ttbdis.2015.08.009 (DOI)000366953400012 ()
    Note

    Funding agencies: Swedish Research Council Branch of Medicine [K2008-58X-14631-06-3]; Medical Research Council of South-East Sweden [FORSS-8967, FORSS-12573, FORSS-29021, FORSS-86911]; EU Interreg IV A project ScandTick [167226]; County Council of Ostergotland [LIO-56191];

    Available from: 2014-03-25 Created: 2014-03-25 Last updated: 2021-12-29Bibliographically approved
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    A STING from a Tick: Epidemiology, Ecology and Clinical Aspects of Lyme Borreliosis
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  • 38.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Cell Biology. Linköping University, Faculty of Health Sciences.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine. Linköping University, Faculty of Health Sciences.
    Börjesson, Stefan
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Nordgren, Johan
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Bergström, Sven
    Ernerudh, Jan
    Linköping University, Department of Clinical and Experimental Medicine, Clinical Immunology. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Center for Diagnostics, Department of Clinical Immunology and Transfusion Medicine.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Infectious Diseases. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Erratum: Prevalence and Diversity of Borrelia Species in Ticks That Have Bitten Humans in Sweden (vol 48, pg 4169, 2010)2011In: Journal of Clinical Microbiology, ISSN 0095-1137, E-ISSN 1098-660X, Vol. 49, no 1, p. 481-481Article in journal (Other academic)
    Abstract [en]

    n/a

  • 39.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Cell Biology. Linköping University, Faculty of Health Sciences.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine. Linköping University, Faculty of Health Sciences.
    Börjesson, Stefan
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Nordgren, Johan
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Bergström, Sven
    Umeå University.
    Ernerudh, Jan
    Linköping University, Department of Clinical and Experimental Medicine, Clinical Immunology. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Centre for Diagnostics, Department of Clinical Immunology and Transfusion Medicine.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Infectious Diseases. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Centre, Department of Infectious Diseases in Östergötland.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Medical Microbiology. Linköping University, Faculty of Health Sciences.
    Prevalence and Diversity of Borrelia Species in Ticks That Have Bitten Humans in Sweden2010In: JOURNAL OF CLINICAL MICROBIOLOGY, ISSN 0095-1137, Vol. 48, no 11, p. 4169-4176Article in journal (Refereed)
    Abstract [en]

    Members of the genus Borrelia are among the most common infectious agents causing tick-borne disease in humans worldwide. Here, we developed a Light Upon eXtension (LUX) real-time PCR assay that can detect and quantify Borrelia species in ticks that have fed on humans, and we applied the assay to 399 such ticks. Borrelia PCR-positive ticks were identified to species level by sequencing the products of conventional PCR performed using Borrelia group-specific primers. There was a 19% prevalence of Borrelia spp. in the detached ticks, and the number of spirochetes per Borrelia PCR-positive tick ranged from 2.0 x 10(2) to 4.9 x 10(5), with a median of 7.8 x 10(3) spirochetes. Adult ticks had a significantly larger number of spirochetes, with a median of 8.4 x 10(4) compared to the median of nymphs of 4.4 x 10(4). Adult ticks also exhibited a higher prevalence of Borrelia (33%) than nymphs (14%). Among the identified species, Borrelia afzelii was found to predominate (61%) and was followed by B. garinii (23%), B. valaisiana (13%), B. burgdorferi sensu stricto (1%), B. lusitaniae (1%), and B. miyamotoi-like (1%). Also, 3% of the ticks were coinfected with multiple strains of B. afzelii. Notably, this is the first report of B. lusitaniae being detected in ticks in Sweden. Our LUX real-time PCR assay proved to be more sensitive than a corresponding TaqMan assay. In conclusion, the novel LUX real-time PCR method is a rapid and sensitive tool for detection and quantification of Borrelia spp. in ticks.

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  • 40.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Lindblom, Pontus
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Sjöwall, Johanna
    Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Heart and Medicine Center, Department of Infectious Diseases. Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine.
    Ahlm, Clas
    Division of Infectious Diseases, Department of Clinical Microbiology, Umeå University, Umeå, Sweden.
    Berglund, Johan
    School of Health Science, Blekinge Institute of Technology, Karlskrona, Sweden.
    Haglund, Mats
    Department of Infectious Diseases, Kalmar County Hospital, Kalmar, Sweden.
    Henningsson, Anna
    Department of Clinical Microbiology, Division of Medical Services, Ryhov County Hospital, Jönkoping, Sweden.
    Nolskog, Peter
    Department of Communicable Disease Control and Prevention, Region Västra Götaland, Skaraborg Hospital, Skövde, Sweden.
    Nordberg, Marika
    The Åland Group for Borrelia Research, Mariehamn, Åland, Finland.
    Nyberg, Clara
    The Åland Group for Borrelia Research, Mariehamn, Åland, Finland.
    Ornstein, Katharina
    Department of Internal Medicine, Hässleholm Hospital, Hässleholm, Sweden/Department of Clinical Sciences, Lund University, Lund, Sweden.
    Nyman, Dag
    The Åland Group for Borrelia Research, Mariehamn, Åland, Finland.
    Ekerfelt, Christina
    Linköping University, Department of Clinical and Experimental Medicine, Division of Inflammation Medicine. Linköping University, Faculty of Health Sciences.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    A prospective study on the incidence of Borrelia infection after a tick bite in Sweden and on the Åland Islands, Finland (2008-2009)2016In: Ticks and Tick-borne Diseases, ISSN 1877-959X, E-ISSN 1877-9603, Vol. 7, no 1, p. 71-79Article in journal (Refereed)
    Abstract [en]

    Lyme borreliosis (LB) is a common and increasing tick-borne disease in Europe. The risk of acquiring a Borrelia infection after a tick bite is not fully known. Therefore, we investigated the incidence of Borrelia infection after a tick bite and if the Borrelia load and/or the duration of tick-feeding influenced the risk of infection. During 2008-2009, ticks and blood samples were collected from 1546 tick-bitten persons from Sweden and the Åland Islands, Finland. Follow-up blood samples were taken three months after the tick bite. The duration of tick feeding was microscopically estimated and Borrelia was detected and quantified in ticks by real-time PCR. Anti-Borrelia antibodies were detected in sera using ELISA assays and immunoblot.

    Even though 28 % of the participants were bitten by a Borrelia-positive tick, only 7.5% (32/428) of them developed a Borrelia infection, half of them LB. All who seroconverted removed “their” ticks significantly later than those who did not. The Borrelia load in the ticks did not explain the risk of seroconversion. Regional as well as gender differences in the Borrelia seroprevalence were found. The risk of developing a Borrelia infection after a bite by a Borrelia-infected tick is small but increases with the duration of tick feeding.

  • 41.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Sweden.
    Jaenson, Thomas G. T.
    Uppsala Univ, Sweden.
    Olsen, Bjorn
    Uppsala Univ, Sweden.
    Waldenstrom, Jonas
    Linnaeus Univ, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Sweden.
    Migratory birds as disseminators of ticks and the tick-borne pathogens Borrelia bacteria and tick-borne encephalitis (TBE) virus: a seasonal study at Ottenby Bird Observatory in South-eastern Sweden2020In: Parasites & Vectors, E-ISSN 1756-3305, Vol. 13, no 1, article id 607Article in journal (Refereed)
    Abstract [en]

    Background: Birds can act as reservoirs of tick-borne pathogens and can also disperse pathogen-containing ticks to both nearby and remote localities. The aims of this study were to estimate tick infestation patterns on migratory birds and the prevalence of different Borrelia species and tick-borne encephalitis virus (TBEV) in ticks removed from birds in south-eastern Sweden. Methods: Ticks were collected from resident and migratory birds captured at the Ottenby Bird Observatory, oland, Sweden, from March to November 2009. Ticks were molecularly identified to species, and morphologically to developmental stage, and the presence of Borrelia bacteria and TBEV was determined by quantitative real-time PCR. Results: A total of 1339 ticks in the genera Haemaphysalis, Hyalomma, and Ixodes was recorded of which I. ricinus was the most abundant species. Important tick hosts were the European robin (Erithacus rubecula), Blackbird (Turdus merula), Tree pipit (Anthus trivialis), Eurasian wren (Troglodytes troglodytes), Common redstart (Phoenicurus phoenicurus), Willow warbler (Phylloscopus trochilus), and Common whitethroat (Sylvia communis). Borrelia bacteria were detected in 25% (285/1,124) of the detached ticks available for analysis. Seven Borrelia species (B. afzelii, B. burgdorferi (s.s.), B. garinii, B. lusitaniae, B. turdi, B. valaisiana, and B. miyamotoi) were identified. B. turdi was recorded for the first time in ticks in Sweden. The number of Borrelia cells per tick ranged from 2.0 x 10(0) to 7.0 x 10(5). B. miyamotoi-containing ticks contained a significantly higher median number of Borrelia cells than B. burgdorferi (s.l.)-containing ticks. B. garinii and B. miyamotoi were the most prevalent Borrelia species in tick larvae. Larvae of I. ricinus with B. garinii were removed from seven bird species, particularly S. communis and A. trivialis, which may suggest that the larvae had contracted the Borrelia bacteria from or via these birds. Also, a high percentage of tick larvae containing B. miyamotoi was removed from E. rubecula. All ticks were negative for TBEV. Conclusions: The results corroborate the view that the contributions of birds to human disease are substantial, particularly as blood hosts for ticks and for their short-, medium-, and long-distance dispersal. Moreover, several ground-foraging bird species appear to be important for the maintenance and dispersal of Borrelia species. The absence of TBEV in the ticks conforms to other similar studies.

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  • 42.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Lindblom, Pontus
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Ernerudh, Jan
    Linköping University, Department of Clinical and Experimental Medicine, Division of Inflammation Medicine. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Center for Diagnostics, Department of Clinical Immunology and Transfusion Medicine.
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Prevalence, Diversity, and Load of Borrelia species in Ticks That Have Fed on Humans in Regions of Sweden and Åland Islands, Finland with Different Lyme Borreliosis Incidences2013In: PLOS ONE, E-ISSN 1932-6203, Vol. 8, no 11, p. e81433-Article in journal (Refereed)
    Abstract [en]

    The incidence of Lyme borreliosis (LB) in a region may reflect the prevalence of Borrelia in the tick population. Our aim was to investigate if regions with different LB incidences can be distinguished by studying the prevalence and diversity of Borrelia species in their respective tick populations. The Borrelia load in a feeding tick increases with the duration of feeding, which may facilitate a transmission of Borrelia Spirochetes from tick to host. Therefore, we also wanted to investigate how the Borrelia load in ticks that have fed on humans varies with the duration of tick feeding. During 2008 and 2009, ticks that had bitten humans were collected from four regions of Sweden and Finland, regions with expected differences in LB incidence. The duration of tick feeding was estimated and Borrelia were detected and quantified by a quantitative PCR assay followed by species determination. Out of the 2,154 Ixodes ricinus ticks analyzed, 26% were infected with Borrelia and seven species were identified. B. spielmanii was detected for the first time in the regions. The tick populations collected from the four regions exhibited only minor differences in both prevalence and diversity of Borrelia species, indicating that these variables alone cannot explain the regions different LB incidences. The number of Borrelia cells in the infected ticks ranged from fewer than ten to more than a million. We also found a lower number of Borrelia cells in adult female ticks that had fed for more than 36 hours, compared to the number of Borrelia cells found in adult female ticks that had fed for less than 36 hours.

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  • 43.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Lindblom, Pontus
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
    Fryland, Linda
    Linköping University, Department of Clinical and Experimental Medicine, Infectious Diseases. Linköping University, Faculty of Health Sciences.
    Nyman, Dag
    Jaenson, Thomas GT
    Uppsala University, Sweden .
    Forsberg, Pia
    Linköping University, Department of Clinical and Experimental Medicine, Infectious Diseases. Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Heart and Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences. Ryhov County Hospital, Jönköping, Sweden .
    Ixodes ricinus ticks removed from humans in Northern Europe: seasonal pattern of infestation, attachment sites and duration of feeding2013In: Parasites & Vectors, E-ISSN 1756-3305, Vol. 6, no 362Article in journal (Refereed)
    Abstract [en]

    BACKGROUND:

    The common tick Ixodes ricinus is the main vector in Europe of the tick-borne encephalitis virus and of several species of the Borrelia burgdorferi sensu lato complex, which are the etiological agents of Lyme borreliosis. The risk to contract bites of I. ricinus is dependent on many factors including the behaviour of both ticks and people. The tick's site of attachment on the human body and the duration of tick attachment may be of clinical importance. Data on I. ricinus ticks, which were found attached to the skin of people, were analysed regarding potentially stage-specific differences in location of attachment sites, duration of tick attachment (= feeding duration), seasonal and geographical distribution of tick infestation in relation to age and gender of the tick-infested hosts.

    METHODS:

    During 2008-2009, 1770 tick-bitten persons from Sweden and the Åland Islands removed 2110 I. ricinus ticks. Participants provided information about the date of tick detection and location on their body of each attached tick. Ticks were identified to species and developmental stage. The feeding duration of each nymph and adult female tick was microscopically estimated based on the scutal and the coxal index.

    RESULTS:

    In 2008, participants were tick-bitten from mid-May to mid-October and in 2009 from early April to early November. The infestation pattern of the nymphs was bimodal whereas that of the adult female ticks was unimodal with a peak in late summer. Tick attachment site on the human body was associated with stage of the tick and gender of the human host. Site of attachment seemed to influence the duration of tick feeding. Overall, 63% of nymphs and adult female ticks were detected and removed more than 24 hours after attachment. Older persons, compared to younger ones, and men, compared to women, removed "their" ticks after a longer period of tick attachment.

    CONCLUSIONS:

    The infestation behaviour of the different tick stages concerning where on the host's body the ticks generally will attach and when such ticks generally will be detected and removed in relation to host age and gender, should be of value for the development of prophylactic methods against tick infestation and to provide relevant advice to people on how to avoid or reduce the risk of tick infestation.

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  • 44.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Lindgren, Per Eric
    Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Medicine and Health Sciences.
    Detection of a novel Lyme borreliosis pathogen.2016In: The Lancet - Infectious diseases, ISSN 1473-3099, E-ISSN 1474-4457, Vol. 16, no 5, p. 511-512Article in journal (Other academic)
  • 45.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty Hosp, Sweden.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty Hosp, Sweden.
    Fransson, Thord
    Swedish Museum Nat Hist, Sweden.
    Grandi, Giulio
    Swedish Univ Agr Sci SLU, Sweden; Natl Vet Inst SVA, Sweden.
    Olsen, Bjoern
    Uppsala Univ, Sweden.
    Nilsson, Kenneth
    Uppsala Univ, Sweden.
    Candidatus Rickettsia Vini DNA in Ticks Collected from Nest Burrows of the European Sand Martin (Riparia riparia) in Sweden2023In: Vector Borne and Zoonotic Diseases, ISSN 1530-3667, E-ISSN 1557-7759Article in journal (Refereed)
    Abstract [en]

    Background: Birds can cross geographical and environmental barriers and thereby facilitate dispersal of tick-borne pathogens both as carriers of infected ticks and as reservoirs of pathogenic microorganisms. Ixodes lividus (Ixodida: Ixodidae) is an endophilic tick in the Palearctic region that is highly specialized on its host, the European sand martin Riparia riparia. The purpose of this study was to determine whether I. lividus ticks sampled from sand martin nests in Sweden carry vector-borne pathogens.Materials and Methods: Fed ticks were collected in the autumns of 2017 and 2019 from the nests of a European sand martin colony in southern Sweden. Ticks were identified morphologically to developmental stage and species and were tested for tick-borne pathogens using PCR-based methods.Results: None of the 41 ticks tested positive for five tick-borne pathogens including Borrelia spp., tick-borne encephalitis virus (TBEV), Neoehrlichia mikurensis, Anaplasma phagocytophilum, and Babesia spp. Thirty-seven (13 females, 23 nymphs and 1 larva) of the 41 ticks tested positive for the gltA gene of Rickettsia spp. The sequences of the 17 kDa and gltA genes were most closely related to Candidatus Rickettsia vini.Conclusion: Our study confirms other reports that I. lividus ticks associated with the European sand martin have high infection prevalence of Ca. R. vini.

  • 46.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Lövmar, Matilda
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    Krogfelt, K. A.
    Statens Serum Inst, Denmark; Roskilde Univ, Denmark.
    Nielsen, H. V.
    Statens Serum Inst, Denmark.
    Forsberg, Pia
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Medicine Center, Department of Infectious Diseases.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Reg Jonkoping Cty, Sweden.
    Clinical/serological outcome in humans bitten by Babesia species positive Ixodes ricinus ticks in Sweden and on the Aland Islands2020In: Ticks and Tick-borne Diseases, ISSN 1877-959X, E-ISSN 1877-9603, Vol. 11, no 4, article id 101455Article in journal (Refereed)
    Abstract [en]

    The risk of contracting babesiosis after a tick bite in Sweden and on the Aland Islands, Finland, is unknown. We investigated clinical and serological outcomes in people bitten by Ixodes ricinus ticks positive for Babesia species. Ticks, blood and questionnaires were obtained from study participants in Sweden and on the Aland Islands. Sixty-five of 2098 (3.1 %) ticks were positive by real-time PCR. Three Babesia species were detected, Babesia microti (n = 33), B. venatorum (n = 27) and B. capreoli (n = 5), the latter species not known to cause human infection. Half (46 %) of the Babesia PCR-positive ticks also contained Borrelia spp. Fifty-three participants bitten by a Babesia PCR-positive tick and a control group bitten by a Babesia PCR-negative tick were tested for B. microti IgG antibodies by IFA. The overall seroprevalence was 4.4 %, but there was no significant difference between the groups. None of the participants seroconverted and no participant with a Babesia PCR-positive tick sought medical care or reported symptoms suggestive of babesiosis. Given the prevalence of Babesia in I. ricinus ticks in southern Sweden and on the Aland Islands, babesiosis should be considered a possible diagnosis in symptomatic residents who seek medical care following tick exposure.

  • 47.
    Wilhelmsson, Peter
    et al.
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Department of Clinical Microbiology, Region Jönköping County, Jönköping, Sweden.
    Pawelczyk, Olga
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Med Univ Silesia, Poland.
    Jaenson, Thomas G. T.
    Uppsala Univ, Sweden.
    Waldenstrom, Jonas
    Linnaeus Univ, Sweden.
    Olsen, Bjorn
    Uppsala Univ, Sweden.
    Forsberg, Pia
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences.
    Lindgren, Per-Eric
    Linköping University, Department of Biomedical and Clinical Sciences, Division of Inflammation and Infection. Linköping University, Faculty of Medicine and Health Sciences. Dept Clin Microbiol, Sweden.
    Three Babesia species in Ixodes ricinus ticks from migratory birds in Sweden2021In: Parasites & Vectors, E-ISSN 1756-3305, Vol. 14, no 1, article id 183Article in journal (Refereed)
    Abstract [en]

    Background Migratory birds can cross geographical and environmental barriers and are thereby able to facilitate transmission of tick-borne pathogens both as carriers of infected ticks and as reservoirs of pathogenic microorganisms. Ixodes ricinus is one of the most abundant tick species in the Northern Hemisphere and a main vector of several Babesia species, some which pose a potential threat to human and animal health. At present only two cases of overt babesiosis in humans have so far been reported in Sweden. To better understand the potential role of birds as disseminators of zoonotic Babesia protozoan parasites, we investigated the presence of Babesia species in ticks removed from migratory birds. Methods Ticks were collected from birds captured at Ottenby Bird Observatory, south-eastern Sweden, from March to November 2009. Ticks were molecularly identified to species, and morphologically to developmental stage, and the presence of Babesia protozoan parasites was determined by real-time PCR. Results In total, 4601 migratory birds of 65 species were examined for tick infestation. Ticks removed from these birds have previously been investigated for the presence of Borrelia bacteria and the tick-borne encephalitis virus. In the present study, a total of 1102 ticks were available for molecular analysis of Babesia protozoan parasites. We found that 2.4% of the ticks examined, all I. ricinus, were positive for mammal-associated Babesia species. Out of all Babesia-positive samples, Babesia venatorum was the most prevalent (58%) species, followed by Babesia microti (38%) and Babesia capreoli (4.0%). B. venatorum and B. capreoli were detected in I. ricinus larvae, whereas B. microti was only present in I. ricinus nymphs. This supports the view that the two first-mentioned species are vertically (transovarially) transmitted in the tick population, in contrast to B. microti. The largest number of Babesia-infected ticks was removed from the common redstart (Phoenicurus phoenicurus) and European robin (Erithacus rubecula). Conclusions This study reveals that Babesia protozoan parasites are present in ticks infesting migratory birds in south-eastern Sweden, which could potentially lead to the dissemination of these tick-borne microorganisms into new areas, thus posing a threat to humans and other mammals.

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