Staff Publications

Staff Publications

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Impact of vertebrate communities on Ixodes ricinus-borne disease risk in forest areas
Takumi, Katsuhisa ; Sprong, Hein ; Hofmeester, Tim R. - \ 2019
Parasites & Vectors 12 (2019)1. - ISSN 1756-3305
Anaplasma phagocytophilum - Borrelia burgdorferi (s.l.) - Borrelia miyamotoi - Ixodes ricinus - Lyme borreliosis - Neoehrlichia mikurensis - Transmission dynamics - Vector-borne disease

Background: The density of questing ticks infected with tick-borne pathogens is an important parameter that determines tick-borne disease risk. An important factor determining this density is the availability of different wildlife species as hosts for ticks and their pathogens. Here, we investigated how wildlife communities contribute to tick-borne disease risk. The density of Ixodes ricinus nymphs infected with Borrelia burgdorferi (sensu lato), Borrelia miyamotoi, Neoehrlichia mikurensis and Anaplasma phagocytophilum among 19 forest sites were correlated to the encounter probability of different vertebrate hosts, determined by encounter rates as measured by (camera) trapping and mathematical modeling. Result: We found that the density of any tick life stage was proportional to the encounter probability of ungulates. Moreover, the density of nymphs decreased with the encounter probability of hare, rabbit and red fox. The density of nymphs infected with the transovarially-transmitted B. miyamotoi increased with the density of questing nymphs and the encounter probability of bank vole. The density of nymphs infected with all other pathogens increased with the encounter probability of competent hosts: bank vole for Borrelia afzelii and N. mikurensis, ungulates for A. phagocytophilum and blackbird for Borrelia garinii and Borrelia valaisiana. The negative relationship we found was a decrease in the density of nymphs infected with B. garinii and B. valaisiana with the encounter probability of wood mouse. Conclusions: Only a few animal species drive the densities of infected nymphs in forested areas. There, foxes and leporids have negative effects on tick abundance, and consequently on the density of infected nymphs. The abundance of competent hosts generally drives the abundances of their tick-borne pathogen. A dilution effect was only observed for bird-associated Lyme spirochetes.[Figure not available: see fulltext.]

Anaplasma phagocytophilum evolves in geographical and biotic niches of vertebrates and ticks
Jaarsma, Ryanne I. ; Sprong, Hein ; Takumi, Katsuhisa ; Kazimirova, Maria ; Silaghi, Cornelia ; Mysterud, Atle ; Rudolf, Ivo ; Beck, Relja ; Földvári, Gábor ; Tomassone, Laura ; Groenevelt, Margit ; Everts, Reinard R. ; Rijks, Jolianne M. ; Ecke, Frauke ; Hörnfeldt, Birger ; Modrý, David ; Majerová, Karolina ; Votýpka, Jan ; Estrada-Peña, Agustín - \ 2019
Parasites & Vectors 12 (2019). - ISSN 1756-3305
Anaplasma phagocytophilum - Ixodidae - Molecular epidemiology - Network analysis - Ticks - Transmission dynamics

Background: Anaplasma phagocytophilum is currently regarded as a single species. However, molecular studies indicate that it can be subdivided into ecotypes, each with distinct but overlapping transmission cycle. Here, we evaluate the interactions between and within clusters of haplotypes of the bacterium isolated from vertebrates and ticks, using phylogenetic and network-based methods. Methods: The presence of A. phagocytophilum DNA was determined in ticks and vertebrate tissue samples. A fragment of the groEl gene was amplified and sequenced from qPCR-positive lysates. Additional groEl sequences from ticks and vertebrate reservoirs were obtained from GenBank and through literature searches, resulting in a dataset consisting of 1623 A. phagocytophilum field isolates. Phylogenetic analyses were used to infer clusters of haplotypes and to assess phylogenetic clustering of A. phagocytophilum in vertebrates or ticks. Network-based methods were used to resolve host-vector interactions and their relative importance in the segregating communities of haplotypes. Results: Phylogenetic analyses resulted in 199 haplotypes within eight network-derived clusters, which were allocated to four ecotypes. The interactions of haplotypes between ticks, vertebrates and geographical origin, were visualized and quantified from networks. A high number of haplotypes were recorded in the tick Ixodes ricinus. Communities of A. phagocytophilum recorded from Korea, Japan, Far Eastern Russia, as well as those associated with rodents had no links with the larger set of isolates associated with I. ricinus, suggesting different evolutionary pressures. Rodents appeared to have a range of haplotypes associated with either Ixodes trianguliceps or Ixodes persulcatus and Ixodes pavlovskyi. Haplotypes found in rodents in Russia had low similarities with those recorded in rodents in other regions and shaped separate communities. Conclusions: The groEl gene fragment of A. phagocytophilum provides information about spatial segregation and associations of haplotypes to particular vector-host interactions. Further research is needed to understand the circulation of this bacterium in the gap between Europe and Asia before the overview of the speciation features of this bacterium is complete. Environmental traits may also play a role in the evolution of A. phagocytophilum in ecotypes through yet unknown relationships.

The genetic diversity of Borrelia afzelii is not maintained by the diversity of the rodent hosts
Coipan, Claudia E. ; Duijvendijk, L.A.G. van; Hofmeester, T.R. ; Takumi, Katsuhisa ; Sprong, H. - \ 2018
Borrelia burgdorferi - Ixodes ricinus larvae - rodents - IGS - ospC - dbpA
Background Small mammals are essential in the enzootic cycle of many tick-borne pathogens (TBP). To understand their contribution to the genetic diversity of Borrelia afzelii, the most prevalent TBP in questing Ixodes ricinus, we compared the genetic variants of B. afzelii at three distinct genetic loci. We chose two plasmid loci, dbpA and ospC, and a chromosomal one, IGS. Results While the larvae that fed on shrews (Sorex sp.) tested negative for B. afzelii, those fed on bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus) showed high infection prevalences of 0.13 and 0.27, respectively. Despite the high genetic diversity within B. afzelii, there was no difference between wood mice and bank voles in the number and types of B. afzelii haplotypes they transmit. Conclusions The genetic diversity in B. afzelii cannot be explained by separate enzootic cycles in wood mice and bank voles.
The genetic diversity of Borrelia afzelii is not maintained by the diversity of the rodent hosts
Coipan, Claudia E. ; Duijvendijk, Gilian L.A. van; Hofmeester, Tim R. ; Takumi, Katsuhisa ; Sprong, Hein - \ 2018
Parasites & Vectors 11 (2018)1. - ISSN 1756-3305
Borrelia burgdorferi (s.l.) - dbpA - IGS - Ixodes ricinus larvae - ospC - Rodents

Background: Small mammals are essential in the enzootic cycle of many tick-borne pathogens (TBP). To understand their contribution to the genetic diversity of Borrelia afzelii, the most prevalent TBP in questing Ixodes ricinus, we compared the genetic variants of B. afzelii at three distinct genetic loci. We chose two plasmid loci, dbpA and ospC, and a chromosomal one, IGS. Results: While the larvae that fed on shrews (Sorex sp.) tested negative for B. afzelii, those fed on bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus) showed high infection prevalences of 0.13 and 0.27, respectively. Despite the high genetic diversity within B. afzelii, there was no difference between wood mice and bank voles in the number and types of B. afzelii haplotypes they transmit. Conclusions: The genetic diversity in B. afzelii cannot be explained by separate enzootic cycles in wood mice and bank voles.

Predicting tick presence by environmental risk mapping
Swart, A. ; Ibañez-Justicia, A. ; Buijs, J. ; Wieren, S.E. van; Hofmeester, T.R. ; Sprong, H. ; Takumi, K. - \ 2014
Frontiers in Public Health 2 (2014). - ISSN 2296-2565
Public health statistics recorded an increasing trend in the incidence of tick bites and erythema migrans (EM) in the Netherlands. We investigated whether the disease incidence could be predicted by a spatially explicit categorization model, based on environmental factors and a training set of tick absence–presence data. Presence and absence of Ixodes ricinus were determined by the blanket-dragging method at numerous sites spread over the Netherlands. The probability of tick presence on a 1 km by 1 km square grid was estimated from the field data using a satellite-based methodology. Expert elicitation was conducted to provide a Bayesian prior per landscape type. We applied a linear model to test for a linear relationship between incidence of EM consultations by general practitioners in the Netherlands and the estimated probability of tick presence. Ticks were present at 252 distinct sampling coordinates and absent at 425. Tick presence was estimated for 54% of the total land cover. Our model has predictive power for tick presence in the Netherlands, tick-bite incidence per municipality correlated significantly with the average probability of tick presence per grid. The estimated intercept of the linear model was positive and significant. This indicates that a significant fraction of the tick-bite consultations could be attributed to the I. ricinus population outside the resident municipality.
Significant increase of Echinococcus multilocularis prevalencein foxes, but no increased predicted risk for humans
Maas, M. ; Dam-Deisz, W.D.C. ; Roon, A.M. van; Takumi, K. ; Giessen, J.W.B. van der - \ 2014
Veterinary Parasitology 206 (2014)3-4. - ISSN 0304-4017 - p. 167 - 172.
human alveolar echinococcosis - red foxes - netherlands - transmission - switzerland - city - dogs
The emergence of the zoonotic tapeworm Echinococcus multilocularis, causative agent ofalveolar echinococcosis (AE), poses a public health risk. A previously designed risk mapmodel predicted a spread of E. multilocularis and increasing numbers of alveolar echinococ-cosis patients in the province of Limburg, The Netherlands. This study was designed todetermine trends in the prevalence and worm burden of E. multilocularis in foxes in a popu-lar recreational area in the southern part of Limburg to assess the risk of infection for humansand to study the prevalence of E. multilocularis in dogs in the adjacent city of Maastricht.Thirty-seven hunted red foxes were tested by the intestinal scraping technique and nestedPCR on colon content. Additionally, 142 fecal samples of domestic dogs from Maastrichtwere analyzed by qPCR for the presence of E. multilocularis.In foxes, a significantly increased prevalence of 59% (95% confidence interval 43–74%)was found, compared to the prevalence of 11% (95% CI 7–18%) in 2005–2006. Average wormburden increased to 37 worms per fox, the highest since the first detection, but consistentwith the prediction about the parasite population for this region. Updated prediction onthe number of AE cases did not lead to an increase in previous estimates of human AE casesup to 2018. No dogs in the city of Maastricht tested positive, but results of questionnairesshowed that deworming schemes were inadequate, especially in dogs that were consideredat risk for infection.
An experimental Toxoplasma gondii dose response challenge model to study therapeutic or vaccine efficacy in cats
Cornelissen, J.B.W.J. ; Giessen, J.W.B. van der; Takumi, K. ; Teunis, P.F.M. ; Wisselink, H.J. - \ 2014
PLoS ONE 9 (2014)9. - ISSN 1932-6203 - 9 p.
crude rhoptry proteins - united-states - tissue cysts - oocysts - bradyzoites - infectivity - tachyzoites - outbreak - animals - humans
High numbers of Toxoplasma gondii oocysts in the environment are a risk factor to humans. The environmental contamination might be reduced by vaccinating the definitive host, cats. An experimental challenge model is necessary to quantitatively assess the efficacy of a vaccine or drug treatment. Previous studies have indicated that bradyzoites are highly infectious for cats. To infect cats, tissue cysts were isolated from the brains of mice infected with oocysts of T. gondii M4 strain, and bradyzoites were released by pepsin digestion. Free bradyzoites were counted and graded doses (1000, 100, 50, 10), and 250 intact tissue cysts were inoculated orally into three cats each. Oocysts shed by these five groups of cats were collected from faeces by flotation techniques, counted microscopically and estimated by real time PCR. Additionally, the number of T. gondii in heart, tongue and brains were estimated, and serology for anti T. gondii antibodies was performed. A Beta-Poisson dose-response model was used to estimate the infectivity of single bradyzoites and linear regression was used to determine the relation between inoculated dose and numbers of oocyst shed. We found that real time PCR was more sensitive than microscopic detection of oocysts, and oocysts were detected by PCR in faeces of cats fed 10 bradyzoites but by microscopic examination. Real time PCR may only detect fragments of T. gondii DNA without the presence of oocysts in low doses. Prevalence of tissue cysts of T. gondii in tongue, heart and brains, and anti T. gondii antibody concentrations were all found to depend on the inoculated bradyzoite dose. The combination of the experimental challenge model and the dose response analysis provides a suitable reference for quantifying the potential reduction in human health risk due to a treatment of domestic cats by vaccination or by therapeutic drug application.
Circulation of four Anaplasma phagocytophilum ecotypes in Europe
Jahfari, S. ; Coipan, E.C. ; Fonville, M. ; Leeuwen, A.D. van; Hengeveld, P. ; Heylen, D. ; Heyman, P. ; Maanen, C. van; Butler, C.M. ; Foldvari, G. ; Szekeres, S. ; Duijvendijk, L.A.G. van; Tack, W. ; Rijks, J.M. ; Giessen, J. van der; Takken, W. ; Wieren, S.E. van; Takumi, K. ; Sprong, H. - \ 2014
Parasites & Vectors 7 (2014)1. - ISSN 1756-3305
candidatus neoehrlichia mikurensis - human granulocytic anaplasmosis - ixodes-ricinus ticks - borrelia-burgdorferi - borne diseases - phylogenetic analyses - sequence-analysis - ehrlichiosis - strains - gene
Background: Anaplasma phagocytophilum is the etiological agent of granulocytic anaplasmosis in humans and animals. Wild animals and ticks play key roles in the enzootic cycles of the pathogen. Potential ecotypes of A. phagocytophilum have been characterized genetically, but their host range, zoonotic potential and transmission dynamics has only incompletely been resolved. Methods. The presence of A. phagocytophilum DNA was determined in more than 6000 ixodid ticks collected from the vegetation and wildlife, in 289 tissue samples from wild and domestic animals, and 69 keds collected from deer, originating from various geographic locations in The Netherlands and Belgium. From the qPCR-positive lysates, a fragment of the groEL-gene was amplified and sequenced. Additional groEL sequences from ticks and animals from Europe were obtained from GenBank, and sequences from human cases were obtained through literature searches. Statistical analyses were performed to identify A. phagocytophilum ecotypes, to assess their host range and their zoonotic potential. The population dynamics of A. phagocytophilum ecotypes was investigated using population genetic analyses. Results: DNA of A. phagocytophilum was present in all stages of questing and feeding Ixodes ricinus, feeding I. hexagonus, I. frontalis, I. trianguliceps, and deer keds, but was absent in questing I. arboricola and Dermacentor reticulatus. DNA of A. phagocytophilum was present in feeding ticks and tissues from many vertebrates, including roe deer, mouflon, red foxes, wild boar, sheep and hedgehogs but was rarely found in rodents and birds and was absent in badgers and lizards. Four geographically dispersed A. phagocytophilum ecotypes were identified, that had significantly different host ranges. All sequences from human cases belonged to only one of these ecotypes. Based on population genetic parameters, the potentially zoonotic ecotype showed significant expansion. Conclusion: Four ecotypes of A. phagocytophilum with differential enzootic cycles were identified. So far, all human cases clustered in only one of these ecotypes. The zoonotic ecotype has the broadest range of wildlife hosts. The expansion of the zoonotic A. phagocytophilum ecotype indicates a recent increase of the acarological risk of exposure of humans and animals.
Geodemographic analysis of Borrelia burgdorferi sensu lato using the 5S-23S rDNA spacer region
Coipan, E.C. ; Fonville, M. ; Tijsse-Klasen, E. ; Giessen, J.W.B. van der; Takken, W. ; Sprong, H. ; Takumi, K. - \ 2013
Infection, Genetics and Evolution 17 (2013). - ISSN 1567-1348 - p. 216 - 222.
ixodes-ricinus ticks - lyme borreliosis - clinical-manifestations - genetic-variability - population-genetics - housekeeping genes - sequence-analysis - bloodmeal source - borne diseases - netherlands
Background: Lyme borreliosis is the predominant tick-borne disease in the Northern hemisphere, with considerable heterogeneity in clinical manifestations. Here, we evaluated one genetic marker for its use in population genetic based analysis. For that we collected molecular and epidemiological records of Borrelia burgdorferi sensu lato isolates from ticks, animals and humans at various sites in The Netherlands and worldwide. Methods: The 5S-23S rDNA (rrfA-rrlB) intergenic spacer region (IGS) from 291 Dutch Borrelia positive ticks was sequenced and compared to Borrelia sequences from GenBank. We estimated several population genetic measures to test the neutrality of the marker. We also assessed the ability of this marker to discriminate between Eurasian Borrelieae at a finer geographical resolution, and to detect population expansion per genospecies. Results: The most prevalent genospecies in The Netherlands was Borrelia afzelii, whereas Borrelia garinii, B. burgdorferi sensu stricto, Borrelia spielmanii and Borrelia valaisiana were found less frequently. The result of the Ewens-Watterson-Slatkin test was consistent with neutral selection of IGS region. Estimated pairwise fixation indices (Fst) were significantly different from zero between The Netherlands, the rest of Europe, Russia and Asia for B. afzelii and Borrelia garinii. Estimated Fu's Fs were significantly negative for B. afzelii and B. garinii. Conclusions: At least seven B. burgdorferi s.l. genospecies circulate in Ixodes ricinus population in The Netherlands. The population genetic analyses of IGS region can resolve subpopulations within a genospecies and detect a large excess of rare genetic variants at the genospecies level. A genetic trace of population expansion for B. afzelii and B. garinii is consistent with the reported increase in Lyme borreliosis incidence in European countries.
Spatiotemporal dynamics of emerging pathogens in questing Ixodes ricinus
Coipan, E.C. ; Jahfari, S. ; Fonville, M. ; Maassen, C.B. ; Giessen, J. van der; Takken, W. ; Takumi, K. ; Sprong, H. - \ 2013
Frontiers in Cellular and Infection Microbiology 3 (2013). - ISSN 2235-2988 - 11 p.
burgdorferi sensu-lato - geographic information-systems - human granulocytic ehrlichiosis - tick-borne diseases - borrelia-burgdorferi - anaplasma-phagocytophilum - lyme borreliosis - human babesiosis - europe - switzerland
Ixodes ricinus transmits Borrelia burgdorferi sensu lato, the etiological agent of Lyme disease. Previous studies have also detected Rickettsia helvetica, Anaplasma phagocytophilum, Neoehrlichia mikurensis, and several Babesia species in questing ticks in The Netherlands. In this study, we assessed the acarological risk of exposure to several tick-borne pathogens (TBPs), in The Netherlands. Questing ticks were collected monthly between 2006 and 2010 at 21 sites and between 2000 and 2009 at one other site. Nymphs and adults were analysed individually for the presence of TBPs using an array-approach. Collated data of this and previous studies were used to generate, for each pathogen, a presence/absence map and to further analyse their spatiotemporal variation. R. helvetica (31.1%) and B. burgdorferi sensu lato (11.8%) had the highest overall prevalence and were detected in all areas. N. mikurensis (5.6%), A. phagocytophilum (0.8%), and Babesia spp. (1.7%) were detected in most, but not all areas. The prevalences of pathogens varied among the study areas from 0 to 64%, while the density of questing ticks varied from 1 to 179/100 m². Overall, 37% of the ticks were infected with at least one pathogen and 6.3% with more than one pathogen. One-third of the Borrelia-positive ticks were infected with at least one other pathogen. Coinfection of B. afzelii with N. mikurensis and with Babesia spp. occurred significantly more often than single infections, indicating the existence of mutual reservoir hosts. Alternatively, coinfection of R. helvetica with either B. afzelii or N. mikurensis occurred significantly less frequent. The diversity of TBPs detected in I. ricinus in this study and the frequency of their coinfections with B. burgdorferi s.l., underline the need to consider them when evaluating the risks of infection and subsequently the risk of disease following a tick bite.
Development of a challenge model for Toxoplansma gondii in cats: assessment of a dose-response for infection
Wisselink, H.J. ; Cornelissen, J.B.W.J. ; Teunis, P.F.M. ; Takumi, K. ; Giessen, J.W.B. van der - \ 2013
In: Abstract Book of Med-Vet-Net Association International Scientific Conference DTU, Lyngby, Denmark, 24-25 June 2013. - - p. 34 - 34.
Circumstantial evidence for an increase in the total number and activity of borrelia-infected ixodes ricinus in the Netherlands.
Sprong, H. ; Hofhuis, A. ; Gassner, F. ; Takken, W. ; Jacobs, F. ; Vliet, A.J.H. van; Ballegooijen, M. van; Giessen, J. van der; Takumi, K. - \ 2012
Parasites & Vectors 5 (2012)5. - ISSN 1756-3305 - 11 p.
tick-borne diseases - burgdorferi sensu-lato - owls strix-aluco - lyme borreliosis - population-dynamics - ixodidae nymphs - endemic area - acari - ecology - risk
BACKGROUND: Between 1994 and 2009, a threefold increase has been observed in consultations of general practitioners for tick bites and Lyme disease in The Netherlands. The objective of this study was to determine whether an increase in the number of questing ticks infected with B. burgdorferi sensu lato is a potential cause of the rise in Lyme disease incidence. METHODS: Historic data on land usage, temperature and wildlife populations were collected and analyzed together with data from two longitudinal field studies on density of questing ticks. Effective population sizes of Borrelia burgdorferi s.l. were calculated. RESULTS: Long-term trend analyses indicated that the length of the annual tick questing season increased as well as the surface area of tick-suitable habitats in The Netherlands. The overall abundances of feeding and reproductive hosts also increased. Mathematical analysis of the data from the field studies demonstrated an increase in mean densities/activities of questing ticks, particularly of larvae between 2006 and 2009. No increase in infection rate of ticks with Borrelia burgdorferi sensu lato was found. Population genetic analysis of the collected Borrelia species points to an increase in B. afzelii and B. garinii populations. CONCLUSIONS: Together, these findings indicate an increase in the total number of Borrelia-infected ticks, providing circumstantial evidence for an increase in the risk of acquiring a bite of a tick infected with B. burgdorferi s.l. Due to the high spatiotemporal variation of tick densities/activities, long-term longitudinal studies on population dynamics of I. ricinus are necessary to observe significant trends.
Public health risk analysis of European bat lyssavirus infection in The Netherlands
Takumi, K. ; Lina, P.H.C. ; Poel, W.H.M. van der; Kramps, J.A. ; Giessen, J.W.B. van der - \ 2009
Epidemiology and Infection 137 (2009). - ISSN 0950-2688 - p. 803 - 809.
rabies - type-1
We present the frequency and the nature of contact incidents of the Serotine bat, Eptesicus serotinus, with humans and with companion animals (specifically cats and dogs), in The Netherlands between 2000 and 2005. Out of 17 bats in bite contact with humans, five tested positive for European bat lyssavirus (EBLV) type 1a. Cats had the most numerous contacts with bats (49 times) but a relatively low number of these bats were EBLV positive (six times). We estimated that the average incidence of human bat rabies infection might be between once per year and once per 700 years, depending mainly on the number of infectious viral particles in bat saliva. The risk of bat rabies is higher between April and October, and in the northern half of the country. This is the first study in Europe describing the risk of human bat rabies after bat contact incidents.
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