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  • 1.
    Blixt, Martin
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Niklasson, Bo
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Sandler, Stellan
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Characterization of β-cell function of pancreatic islets isolated from bank voles developing glucose intolerance/diabetes: an animal model showing features of both type 1 and type 2 diabetes mellitus, and a possible role of the Ljungan virus2007In: General and Comparative Endocrinology, ISSN 0016-6480, E-ISSN 1095-6840, Vol. 154, no 1-3, p. 41-47Article in journal (Refereed)
    Abstract [en]

    Bank voles (Clethrionomys glareolus) kept in captivity develop diabetes mellitus to a significant extent. Also in wild bank voles, elevated blood glucose has been observed. A newly isolated picornavirus named Ljungan virus (LV) has been found in the pancreas of these bank voles. Moreover, LV infection in combination with environmental factors may cause glucose intolerance/diabetes (GINT/D) in normal mice. The aim of the present study was to investigate the functional characteristics of pancreatic islets, isolated from bank voles, bred in the laboratory but considered LV infected. About 20% of all males and females were classified as GINT/D following a glucose tolerance test. Of these animals the majority had become diabetic by 20 weeks of age, with a tendency towards an earlier onset in the males. GINT/D animals had increased serum insulin levels. Islets were tested on the day of isolation (day 0) and after 1 week of culture for their insulin content and their capacity to synthesize (pro)insulin, secrete insulin and metabolize glucose. Functional differences could be observed between normal and GINT/D animals as well as between genders. An elevated basal insulin secretion was observed on day 0 indicating β-cell dysfunction among islets isolated from diabetic males. In vitro culture could reverse some functional changes. The increased serum insulin level and the increased basal islet insulin secretion may suggest that the animals had developed a type 2 diabetes-like condition. It is likely that the putative stress imposed in the laboratory, maybe in combination with LV infection, can lead to an increased functional demand on the β-cells.

  • 2. Ekström, Jens-Ola
    et al.
    Tolf, Conny
    Fahlgren, Camilla
    Johansson, E Susanne
    Arbrandt, Gustav
    Niklasson, Bo
    Edman, Kjell-A
    Lindberg, A Michael
    Replication of Ljungan virus in cell culture: the genomic 5'-end, infectious cDNA clones and host cell response to viral infections2007In: Virus Research, ISSN 0168-1702, E-ISSN 1872-7492, Vol. 130, no 1-2, p. 129-139Article in journal (Refereed)
    Abstract [en]

    Ljungan virus (LV) is a picornavirus recently isolated from bank voles (Clethrionomys glareolus). The previously uncharacterised 5'-end sequence of the LV genome was determined. Infectious cDNA clones were constructed of the wild type LV prototype strain 87-012 and of the cytolytically replicating cell culture adapted variant 87-012G. Virus generated from cDNA clones showed identical growth characteristics as uncloned virus stocks. Cell culture adapted LV, 87-012G, showed a clear cytopathic effect (CPE) at 3-4 days post-infection (p.i.). Virus titers, determined by plaque titration, increased however only within the first 18h p.i. Replication of LV (+) strand RNA was determined by real-time PCR and corresponded in time with increasing titers. In contrast, the amounts of the replication intermediate, the (-) strand, continued to increase until the cells showed CPE. This indicates separate controlling mechanisms for replication of LV (+) and (-) genome strands. Replication was also monitored by immunofluorescence (IF) staining. IF staining of both prototype 87-012 and the CPE causing 87-012G showed groups of 5-25 infected cells at 48h p.i., suggesting a, for picornaviruses, not previously described direct cell-to-cell transmission.

  • 3. Escadafal, Camille
    et al.
    Avsic-Zupanc, Tatjana
    Vapalahti, Olli
    Niklasson, Bo
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Teichmann, Anette
    Niedrig, Matthias
    Donoso-Mantke, Oliver
    Second External Quality Assurance Study for the Serological Diagnosis of Hantaviruses in Europe2012In: PLoS Neglected Tropical Diseases, ISSN 1935-2735, Vol. 6, no 4, p. e1607-Article in journal (Refereed)
    Abstract [en]

    Hantaviruses are endemic throughout the world and hosted by rodents and insectivores. Two human zoonoses, hemorrhagic fever with renal syndrome (HFRS) and hantavirus pulmonary syndrome (HPS), are caused by hantaviruses and case fatality rates have reached 12% for HFRS and 50% for HPS in some outbreaks. Symptomatic hantavirus infections in Europe are summarised as HFRS mainly due to Puumala, Dobrava-Belgrade and Saaremaa virus. While HFRS has an overall low incidence in Europe, the number of cases varies from 100 per year in all Eastern and Southern Europe up to 1,000 per year only in Finland. To assess the quality of hantavirus diagnostics, the European Network for the Diagnostics of 'Imported'' Viral Diseases (ENIVD) organised a first external quality assurance (EQA) in 2002. The purpose of this second EQA study is to collect updated information on the efficiency and accurateness of hantavirus serological methods applied by expert laboratories. A serum panel of 14 samples was sent to 28 participants in Europe of which 27 sent results. Performance in hantavirus diagnosis varied not only on the method used but also on the laboratories and the subclass of antibodies tested. Commercial and in-house assays performed almost equally. Enzyme immunoassays were mainly used but did not show the best performances while immunoblot assays were the less employed and showed overall better performances. IgM antibodies were not detected in 61% of the positive IgM samples and IgM detection was not performed by 7% of the laboratories indicating a risk of overlooking acute infections in patients. Uneven performances using the same method is indicating that there is still a need for improving testing conditions and standardizing protocols.

  • 4. Litzba, Nadine
    et al.
    Zelena, Hana
    Kreil, Thomas R.
    Niklasson, Bo
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Kuehlmann-Rabens, Ilona
    Remoli, Maria Elena
    Niedrig, Matthias
    Evaluation of Different Serological Diagnostic Methods for Tick-Borne Encephalitis Virus: Enzyme-Linked Immunosorbent, Immunofluorescence, and Neutralization Assay2014In: Vector Borne and Zoonotic Diseases, ISSN 1530-3667, E-ISSN 1557-7759, Vol. 14, no 2, p. 149-159Article in journal (Refereed)
    Abstract [en]

    Tick-borne encephalitis (TBE) is a zoonotic disease, transmitted mainly by the bite of ticks. The TBE virus (TBEV) belongs to the family Flaviviridae, genus Flavivirus and is able to cause meningoencephalitis. For serological TBEV detection, the neutralization test (NT) is the most specific assay available. Different NT protocols are used in the laboratories, and until now the performance of these NTs has never been tested in an external quality assessment (EQA). In this EQA, we compared the results of eight European laboratories in detecting 17 samples (11 TBEV positive, five flavivirus cross reactive, and one negative sample) by NT. Furthermore, 14 of these EQA samples and 15 additional samples were tested in different commercial assays: 15 immunoglobulin G (IgG) enzyme-linked immunosorbent assays (ELISAs) and an immunofluorescence assay (IFA). Four laboratories showed a good NT EQA performance, whereas four laboratories had some sensitivity problems. Additionally, two of these laboratories showed a lack in specificity, misidentifying a dengue-positive sample as TBEV positive. The comparison of the commercial ELISAs revealed a high sensitivity in all assays, but as expected for IgG, the ELISAs showed a high degree of flavivirus cross reactivity. The assessment of Vienna Units in some of the ELISAs revealed deviations in the standards used by the different companies. Therefore, these standards should be revised. Generally, in this EQA, we found that reliable NT protocols are used in most of the laboratories, and the evaluation of the IgG ELISAs and the IFA showed a good agreement.

  • 5.
    Magnusson, M.
    et al.
    Swedish Univ Agr Sci, Dept Wildlife Fish & Environm Studies, SE-90183 Umea, Sweden..
    Ecke, F.
    Swedish Univ Agr Sci, Dept Wildlife Fish & Environm Studies, SE-90183 Umea, Sweden.;Sweden Univ Agr Sci, Dept Aquat Sci & Assessment, SE-75007 Uppsala, Sweden..
    Khalil, H.
    Swedish Univ Agr Sci, Dept Wildlife Fish & Environm Studies, SE-90183 Umea, Sweden..
    Olsson, G.
    Swedish Univ Agr Sci, Dept Wildlife Fish & Environm Studies, SE-90183 Umea, Sweden..
    Evander, M.
    Umea Univ, Dept Clin Microbiol, SE-90185 Umea, Sweden..
    Niklasson, Bo
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Hornfeldt, B.
    Swedish Univ Agr Sci, Dept Wildlife Fish & Environm Studies, SE-90183 Umea, Sweden..
    Spatial and temporal variation of hantavirus bank vole infection in managed forest landscapes2015In: Ecosphere, ISSN 2150-8925, E-ISSN 2150-8925, Vol. 6, no 9, article id 163Article in journal (Refereed)
    Abstract [en]

    Zoonoses are major contributors to emerging infectious diseases globally. Hemorrhagic fever with renal syndrome (HFRS) is a zoonosis caused by rodent-borne hantaviruses. In Europe, Puumala hantavirus (PUUV) carried and shed by the bank vole (Myodes glareolus), is the most common cause of HFRS. We explore the relationship of PUUV infection in bank voles, as measured by PUUV antibody detection, with habitat and landscape scale properties during two successive vole cycles in boreal Sweden. Our analysis revealed that PUUV infection in the population was not uniform between cycles and across different landscapes. The mean density index of PUUV antibody positive and negative bank voles were highest in old forest, second highest in cut-over forest (approx. 0-30 years old) and lowest on mires. Most importantly, old forest was the core habitat, where PUUV antibody positive bank voles were found through the low density phase and the transition between successive vole cycles. In spring, occurrence of antibody positive voles was negatively related to the proportion of cut-over forest in the surrounding landscape, suggesting that large scale human induced land-use change altered the occurrence of PUUV infection in voles which has not been shown before. Dependence of PUUV infection on habitat and landscape structure, and the variation in infection load within and between cycles are of importance for human risk assessment.

  • 6.
    Niklasson, Bo
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    The relationship of vehicle and concentration for imidazolidinylurea, with attention to formaldehyde allergy status2006In: Dermatitis, ISSN 1710-3568, E-ISSN 2162-5220, Vol. 17, no 2, p. 93-Article in journal (Other academic)
  • 7.
    Niklasson, Bo
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Hultman, T
    Kallies, R
    Niedrig, M
    Nilsson, R
    Berggren, P-O
    Juntti-Berggren, L
    Efendic, S
    Lernmark, A
    Klitz, W
    The BioBreeding rat diabetes model is infected with Ljungan virus2007In: Diabetologia, ISSN 0012-186X, E-ISSN 1432-0428, Vol. 50, no 7, p. 1559-1560Article in journal (Refereed)
  • 8.
    Niklasson, Bo
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Nyholm, Erik
    Feinstein, Ricardo E.
    Samsioe, Annika
    Hörnfeldt, Birger
    Diabetes and myocarditis in voles and lemmings at cyclic peak densities--induced by Ljungan virus?2006In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 150, no 1, p. 1-7Article in journal (Refereed)
    Abstract [en]

    Although it is well-documented from theoretical studies that pathogens have the capacity to generate cycles, the occurrence and role of pathogens and disease have been poorly empirically studied in cyclic voles and lemmings. In screening for the occurrence of disease in cyclic vole and lemming populations, we found that a high proportion of live-trapped Clethrionomys glareolus, C. rufocanus, Microtus agrestis and Lemmus lemmus at high collective peak density, shortly before the decline, suffered from diabetes or myocarditis in northern Scandinavia. A high frequency of animals had abnormal blood glucose (BG) levels at the time of trapping (5-33%). In contrast, C. rufocanus individuals tested at a much lower overall density, and at an earlier stage relative to the decline in the following cycle, showed normal BG concentrations. However, a high proportion (43%) of a sample of these individuals kept in captivity developed clinical diabetes within five weeks, as determined by BG levels and a glucose tolerance test performed at that later time. A new picornavirus isolated from the rodents, Ljungan virus (LV), was assumed to cause the diseases, as LV-induced diabetes and myocarditis, as well as encephalitis and fetal deaths, were observed in laboratory mice. We hypothesize that LV infection significantly affects morbidity and mortality rates in the wild, either directly or indirectly, by predisposing the rodents to predation, and is at least involved in causing the regular, rapid population declines of these cyclic voles and lemmings. Increased stress at peak densities is thought to be an important trigger for the development of disease, as the occurrence of disease in laboratory mice has been found to be triggered by introducing stress to LV-infected animals.

  • 9.
    Niklasson, Bo
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Samsioe, A.
    Blixt, Martin
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Sandler, Stellan
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Sjöholm, A.
    Lagerquist, E.
    Lernmark, Å.
    Klitz, W.
    Prenatal viral exposure followed by adult stress produces glucose intolerance in a mouse model2006In: Diabetologia, ISSN 0012-186X, E-ISSN 1432-0428, Vol. 49, no 9, p. 2192-2199Article in journal (Refereed)
    Abstract [en]

    Aims/hypothesis: It has been suggested that the uterine environment may influence metabolic disease occurring later in adult life, and that adult stress may promote disease outcome. Using a mouse model, we tested whether in utero exposure to Ljungan virus (LV) followed by adult exposure to stress produces diabetes. The influence of the timing of viral exposure over the course of pregnancy was also tested.

    Materials and methods: Pregnant CD-1 mice were exposed i.p. to LV on pregnancy days 4, 8, 12 or 17. Adult male mice from these pregnancies were stressed by being kept in shared cages. Stress only, LV exposure in utero only, and no-stress/no virus exposure groups were also followed. Outcome variables included bodyweight, epididymal fat weight, baseline glucose, glucose tolerance tests (60 and 120 min) and serum insulin.

    Results: We demonstrated that male mice developed a type 2-like diabetes, including obesity, as adults if infected during pregnancy with LV. Diabetes at the age of 11 weeks was more severe in mice whose mothers were infected earlier than in those whose mothers were infected later in pregnancy. Only animals infected in utero and kept under stress developed diabetes; infection or stress alone did not cause disease.

    Conclusions/interpretation: This work demonstrates that a type 2 diabetes-like disease can be virus-induced in a mouse model. Early in utero viral insults can set the stage for disease occurring during adult life, but the final manifestation of diabetes is dependent on the combination of early viral exposure and stress in adult life.

  • 10.
    Niklasson, Bo
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Samsioe, Annika
    Papadogiannakis, Nikos
    Kawecki, Anne
    Hörnfeldt, Birger
    Saade, George R
    Klitz, William
    Association of zoonotic Ljungan virus with intrauterine fetal deaths2007In: Birth defects research. Clinical and molecular teratology, ISSN 1542-0752, E-ISSN 1542-0760, Vol. 79, no 6, p. 488-493Article in journal (Refereed)
    Abstract [en]

    BACKGROUND: It has recently been shown that Ljungan virus (LV) is associated with disease in its wild rodent reservoir. In addition, it has been demonstrated that LV causes malformations and perinatal death in a mouse model. The question was therefore raised whether LV is a zoonotic agent in humans. METHODS: Population fluctuations of native rodents in Sweden were compared to the incidence of intrauterine fetal deaths (IUFDs) using the Swedish national hospitalization database. Formalin-fixed tissues from cases of IUFD were investigated using LV-specific immunohistochemistry. RESULTS: Variation in the incidence of IU-FDs closely tracked the fluctuations in native rodent populations. LV was detected in the brain tissue in 4 of 10 cases of IUFDs investigated by immunochemistry. LV was also detected in the placenta in 5 of the 10 IUFD cases, but in none of 20 placentas from normal pregnancies. CONCLUSIONS: LV may play an important role in IUFDs.

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