Publications by authors named "Joke W B van der Giessen"

31 Publications

Effectiveness and costs of interventions to reduce the within-farm Toxoplasma gondii seroprevalence on pig farms in the Netherlands.

Porcine Health Manag 2021 Jul 26;7(1):44. Epub 2021 Jul 26.

Vion Food Group, Boxtel, The Netherlands.

Background: The parasite Toxoplasma gondii (T. gondii) is recognized as one of the major foodborne pathogens with a high human disease burden. To control T. gondii infections in pigs, European Food Safety Agency (EFSA) advises serological testing of pigs and audits of pig farms to identify risk factors for T. gondii infection. In line with this approach, the aim of the current study was to assess the effectiveness and costs of intervention measures implemented to reduce the T. gondii seroprevalence on finishing pig farms in the Netherlands. A crossover clinical trial was conducted at five case farms were their own control and the cross-over moment was the implementation of interventions to reduce risk factors. Each of the case farms had a farm-specific intervention strategy with one principal intervention measure (neutering of cats, professional rodent control or covering food storage).

Results: All finishing pig farms (n = 5) showed a reduction in T. gondii seroprevalence within one year of implementing the intervention strategy. Cat neutering (n = 3) and feed coverage (n = 1) showed statistically significant reductions in seroprevalence. Rodent control (n = 1) did not show a statistically significant reduction. The estimated reduction in seroprevalence in response to the neutering of cats and feed coverage were 67 and 96 %, respectively.

Conclusions: Our work demonstrates that it is possible to reduce the within-farm T. gondii seroprevalence within one year after interventions were implemented to reduce T. gondii risk factors. This information is essential and encouraging for policy makers, food business operators, and farmers to implement in their risk assessment and to apply to food safety control systems.
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http://dx.doi.org/10.1186/s40813-021-00223-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8311922PMC
July 2021

Mining Public Metagenomes for Environmental Surveillance of Parasites: A Proof of Principle.

Front Microbiol 2021 30;12:622356. Epub 2021 Jun 30.

Centre for Zoonoses and Environmental Microbiology, National Institute for Public Health and the Environment, Bilthoven, Netherlands.

Parasites often have complex developmental cycles that account for their presence in a variety of difficult-to-analyze matrices, including feces, water, soil, and food. Detection of parasites in these matrices still involves laborious methods. Untargeted sequencing of nucleic acids extracted from those matrices in metagenomic projects may represent an attractive alternative method for unbiased detection of these pathogens. Here, we show how publicly available metagenomic datasets can be mined to detect parasite specific sequences, and generate data useful for environmental surveillance. We use the protozoan parasite as a test organism, and show that detection is influenced by the reference sequence chosen. Indeed, the use of the whole genome yields high sensitivity but low specificity, whereas specificity is improved through the use of signature sequences. In conclusion, querying metagenomic datasets for parasites is feasible and relevant, but requires optimization and validation. Nevertheless, this approach provides access to the large, and rapidly increasing, number of datasets from metagenomic and meta-transcriptomic studies, allowing unlocking hitherto idle signals of parasites in our environments.
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http://dx.doi.org/10.3389/fmicb.2021.622356DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8278238PMC
June 2021

Mathematical modelling of transmission: A systematic review.

Food Waterborne Parasitol 2021 Mar 9;22:e00102. Epub 2020 Dec 9.

Centre for Infectious Disease Control - Zoonoses and Environmental Microbiology, National Institute for Public Health and the Environment, 3720, BA, Bilthoven, the Netherlands.

Background: is a ubiquitous protozoan parasite that can infect virtually all warm-blooded animals. It is the causative agent of toxoplasmosis, a significant public health issue worldwide. Mathematical models are useful to study the transmission dynamics of infection in different settings, and may be used to compare the effectiveness of prevention measures.

Methods: To obtain an overview of existing mathematical models for transmission of , a systematic review was undertaken. The review was conducted according to an a priori protocol and the results were reported according to the PRISMA guidelines. Specific search terms were developed and used in the search of three databases (Scopus, PubMed, and Embase).

Results: In total, 484 unique records were retrieved from the systematic search. Among them, 15 studies that used mathematical models to study the transmission of . These studies were categorized into four groups based on the primary aims: dynamics of transmission ( = 8), intervention ( = 5), spatial distribution ( = 1), and outbreak investigation (n = 1).

Conclusions: Considering the high disease burden caused by , the number of studies using mathematical models to understand the transmission dynamics of this parasite and to evaluate the effectiveness of intervention measures was only 15. This systematic review provides an overview of existing mathematical models and identifies the data gaps for model building. The results from this study can be helpful for further development of mathematical models and improved understanding of the transmission dynamics of infection.
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http://dx.doi.org/10.1016/j.fawpar.2020.e00102DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7753131PMC
March 2021

Source attribution of human echinococcosis: A systematic review and meta-analysis.

PLoS Negl Trop Dis 2020 06 22;14(6):e0008382. Epub 2020 Jun 22.

Department of Biomedical Science, Institute of Tropical Medicine, Belgium.

Background: A substantial proportion of echinococcosis transmission to humans via contamination of food has been assumed. However, the relative importance of food as a transmission vehicle has previously been estimated through expert opinion rather than empirical data.

Objective: To find and evaluate empirical data that could be used to estimate the source attribution of echinococcosis, in particular the proportion that is transmitted through contaminated food.

Methods: A systematic review was undertaken to identify reports on the risk factors for human cystic (CE) and alveolar (AE) echinococcosis. Data bases searched included PubMed, Scopus, Web of Knowledge, Cab Direct, Science Direct, Google Scholar, eLIBRARY.RU, CyberLeninka, CNKI and VIP. Search terms included Echinococc*, hydatid, epidemiology, logistic regression, risk factors, odds ratio, relative risk, risk factors. Reports, including grey literature where available, that had suitable data were selected and data were extracted. The main pathways of transmission were hypothesised to be contact with the definitive host, contaminated water, contaminated food and contaminated environment (other than food). For each study the attributable fraction for these potential sources of infection was calculated from the data presented. A meta-analysis was then undertaken to obtain pooled estimates for the relative contribution of these transmission pathways.

Results: Data from 28 cross-sectional studies and 14 case-control studies were extracted. There was strong evidence for transmission by direct contact with dogs for both CE and AE. The estimated attributable fractions were 26.1% (CI 13.8%-39.6%) and 34.4% (CI 20.7% -48.2%) respectively. Transmission through contaminated water was estimated to be responsible for approximately 29.4% (CI 12.1%-51.7%) for CE and 24.8% (CI 10.6% to 42.6%) for AE. Contaminated food may be responsible for approximately 23.4% of CE cases (CI 2.1%-47.3%). Globally, there was insufficient evidence to conclude AE can be transmitted by food, although case control studies from low human incidence areas suggested that possibly 32.5% (CI 10.0%-53.2%) could be transmitted by food. There was also insufficient evidence that direct contact with foxes was a significant source of human disease. There were no suitable studies with a risk of environmental contact reported, but the residual attributable fraction thatwould likely include this pathway was approximately 21.1% for CE and 11.1% for AE.

Conclusions: The results support the hypothesis that dog contact and drinking contaminated water are major pathways of transmission of both CE and AE. For contaminated food, the results are less consistent, but suggest that it is an important transmission pathway and provide better evidence than expert elicitations as previously used.
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http://dx.doi.org/10.1371/journal.pntd.0008382DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7332091PMC
June 2020

The effect of salting on Toxoplasma gondii viability evaluated and implemented in a quantitative risk assessment of meat-borne human infection.

Int J Food Microbiol 2020 Feb 30;314:108380. Epub 2019 Oct 30.

Centre for Infectious Disease Control - Zoonoses and Environmental Microbiology, National Institute for Public Health and the Environment, 3720 BA Bilthoven, the Netherlands. Electronic address:

The protozoan parasite Toxoplasma gondii can infect all warm-blooded animals and it causes the disease toxoplasmosis. Meat containing viable T. gondii tissue cysts is considered one of the main sources of human infection. The relative importance of the different types of meat depends, not only on the prevalence of T. gondii infection in the different livestock species, but also on consumed volumes and preparation habits. To take these factors into account and to estimate the relative contribution of different meat products to human infection, a quantitative risk assessment model for meat-borne T. gondii infection was previously developed. However, at the time, the effect of salting on parasite viability was estimated based on a single experiment. In recent years, data using salting methods that are more in line with processing of meat products have come available. Literature data on the effect of salting on T. gondii viability were collected and used to fit a predictive model. In addition to the new salting model, a lower concentration of bradyzoites in cattle, more specific heating profiles, and more recent consumption data were implemented in the QMRA model for meat-borne T. gondii infection in the Netherlands. Results show that beef remains the most important source, as it contributed 84% of the total number of predicted infections in the Dutch population, followed by pork (12%), mutton (3.7%), lamb (0.2%) pork/beef mixed products (0.1%), and veal (0.01%). The predicted number of T. gondii infections is reasonably in line with epidemiological data. At the product level, filet americain (a raw beef spread) alone contributed 80% of the total predicted infections in the base model, but scenario analyses demonstrate that its contribution is highly dependent on the salting parameters. A clear identification of the most risky meat products is important, as interventions focussing on these products could have a great impact on reducing T. gondii disease burden in the Netherlands. For that reason, it is important that the effects of salting and other processing methods are evaluated in line with industrial processing and incorporated in quantitative risk assessment models for meat-borne toxoplasmosis.
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http://dx.doi.org/10.1016/j.ijfoodmicro.2019.108380DOI Listing
February 2020

A social cost-benefit analysis of two One Health interventions to prevent toxoplasmosis.

PLoS One 2019 10;14(5):e0216615. Epub 2019 May 10.

National Institute for Public Health and the Environment, Bilthoven, the Netherlands.

In the Netherlands, toxoplasmosis ranks second in disease burden among foodborne pathogens with an estimated health loss of 1,900 Disability Adjusted Life Years and a cost-of-illness estimated at €45 million annually. Therefore, effective and preferably cost-effective preventive interventions are warranted. Freezing meat intended for raw or undercooked consumption and improving biosecurity in pig farms are promising interventions to prevent Toxoplasma gondii infections in humans. Putting these interventions into practice would expectedly reduce the number of infections; however, the net benefits for society are unknown. Stakeholders bearing the costs for these interventions will not necessary coincide with the ones having the benefits. We performed a Social Cost-Benefit Analysis to evaluate the net value of two potential interventions for the Dutch society. We assessed the costs and benefits of the two interventions and compared them with the current practice of education, especially during pregnancy. A 'minimum scenario' and a 'maximum scenario' was assumed, using input parameters with least benefits to society and input parameters with most benefits to society, respectively. For both interventions, we performed different scenario analyses. The freezing meat intervention was far more effective than the biosecurity intervention. Despite high freezing costs, freezing two meat products: steak tartare and mutton leg yielded net social benefits in both the minimum and maximum scenario, ranging from €10.6 million to €31 million for steak tartare and €0.6 million to €1.5 million for mutton leg. The biosecurity intervention would result in net costs in all scenarios ranging from €1 million to €2.5 million, due to high intervention costs and limited benefits. From a public health perspective (i.e. reducing the burden of toxoplasmosis) and the societal perspective (i.e. a net benefit for the Dutch society) freezing steak tartare and leg of mutton is to be considered.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0216615PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6510435PMC
January 2020

Seroprevalence of hantaviruses and in muskrat and coypu trappers in the Netherlands, 2016.

Infect Ecol Epidemiol 2018 16;8(1):1474707. Epub 2018 May 16.

Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands.

Seoul orthohantavirus (SEOV) and  spp. are zoonotic pathogens with rats as main reservoir. Recently, the presence of SEOV in brown rats was reported in one region in the Netherlands. Brown rats are a frequent bycatch in traps placed to catch muskrats () and coypus (), and thus are a potential health risk for trappers. It was our aim to determine the seroprevalence of orthohantavirus, specifically SEOV, and  spp in Dutch trappers. Participating trappers provided serum samples and completed an online questionnaire. The serum was tested for the presence of antibodies against six orthohantaviruses and eight  serovars. Two hundred-sixty trappers completed the online questionnaire (65%), and 246 (61%) and 162 (40%) serum samples were tested for relevant orthohantaviruses and  spp., respectively. The seroprevalence of Puumala orthohantavirus in Dutch trappers was 0.4% (95% CI: 0.1-2.3%). None of the participants tested positive for SEOV. The seroprevalence of leptospirosis was 1.2% (95% CI: 0.3-4.4%), although  spp. are present in brown rats in the Netherlands. The results indicate that the infections with orthohantaviruses and leptospires is low for muskrat and coypu trappers.
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http://dx.doi.org/10.1080/20008686.2018.1474707DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5965032PMC
May 2018

BRUCELLA PINNIPEDIALIS IN GREY SEALS ( HALICHOERUS GRYPUS) AND HARBOR SEALS ( PHOCA VITULINA) IN THE NETHERLANDS.

J Wildl Dis 2018 07 26;54(3):439-449. Epub 2018 Apr 26.

1   Wageningen Bioveterinary Research of Wageningen University and Research (WBVR), Edelhertweg 15, 8200 AB Lelystad, the Netherlands.

Brucellosis is a zoonotic disease with terrestrial or marine wildlife animals as potential reservoirs for the disease in livestock and human populations. The primary aim of this study was to assess the presence of Brucella pinnipedialis in marine mammals living along the Dutch coast and to observe a possible correlation between the presence of B. pinnipedialis and accompanying pathology found in infected animals. The overall prevalence of Brucella spp. antibodies in sera from healthy wild grey seals ( Halichoerus grypus; n=11) and harbor seals ( Phoca vitulina; n=40), collected between 2007 and 2013 ranged from 25% to 43%. Additionally, tissue samples of harbor seals collected along the Dutch shores between 2009 and 2012, were tested for the presence of Brucella spp. In total, 77% (30/39) seals were found to be positive for Brucella by IS 711 real-time PCR in one or more tissue samples, including pulmonary nematodes. Viable Brucella was cultured from 40% (12/30) real-time PCR-positive seals, and was isolated from liver, lung, pulmonary lymph node, pulmonary nematode, or spleen, but not from any PCR-negative seals. Tissue samples from lung and pulmonary lymph nodes were the main source of viable Brucella bacteria. All isolates were typed as B. pinnipedialis by multiple-locus variable number of tandem repeats analysis-16 clustering and matrix-assisted laser desorption ionization-time of flight mass spectrometry, and of sequence type ST25 by multilocus sequence typing analysis. No correlation was observed between Brucella infection and pathology. This report displays the isolation and identification of B. pinnipedialis in marine mammals in the Dutch part of the Atlantic Ocean.
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http://dx.doi.org/10.7589/2017-05-097DOI Listing
July 2018

Seroprevalence of Toxoplasma gondii in pregnant women and livestock in the mainland of China: a systematic review and hierarchical meta-analysis.

Sci Rep 2018 04 18;8(1):6218. Epub 2018 Apr 18.

Centre for Infectious Disease Control - Zoonoses and Environmental Microbiology, National Institute for Public Health and the Environment, 3720 BA, Bilthoven, Netherlands.

Primary Toxoplasma gondii infection in pregnant women may result in abortion, stillbirth, or lifelong disabilities of the unborn child. One of the main transmission routes to humans is consumption of raw or undercooked meat containing T. gondii tissue cysts. We aim to determine and compare the regional distribution of T. gondii seroprevalence in pregnant women and meat-producing livestock in China through a systematic literature review. A total of 272 eligible publications were identified from Medline, Scopus, Embase and China National Knowledge Infrastructure. Apparent and true seroprevalence were analysed by region using a novel Bayesian hierarchical model that allowed incorporating sensitivity and specificity of the applied serological assays. The true seroprevalence of T. gondii in pregnant women was 5.0% or less in seven regions of China. The median of the regional true seroprevalences in pigs (24%) was significantly higher than in cattle (9.5%), but it was not significantly higher than in chickens (20%) and small ruminants (20%). This study represents the first use of a Bayesian hierarchical model to obtain regional true seroprevalence. These results, in combination with meat consumption data, can be used to better understand the contribution of meat-producing animals to human T. gondii infection in China.
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http://dx.doi.org/10.1038/s41598-018-24361-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5906581PMC
April 2018

Zoonotic bacteria and parasites found in raw meat-based diets for cats and dogs.

Vet Rec 2018 01;182(2):50

Division of Veterinary Public Health, Faculty of Veterinary Medicine, Institute for Risk Assessment Sciences, Utrecht University, Utrecht, The Netherlands.

Feeding raw meat-based diets (RMBDs) to companion animals has become increasingly popular. Since these diets may be contaminated with bacteria and parasites, they may pose a risk to both animal and human health. The purpose of this study was to test for the presence of zoonotic bacterial and parasitic pathogens in Dutch commercial RMBDs. We analysed 35 commercial frozen RMBDs from eight different brands. serotype O157:H7 was isolated from eight products (23 per cent) and extended-spectrum beta-lactamases-producing was found in 28 products (80 per cent). was present in 19 products (54 per cent), other species in 15 products (43 per cent) and species in seven products (20 per cent). Concerning parasites, four products (11 per cent) contained and another four (11 per cent) In two products (6 per cent) was found. The results of this study demonstrate the presence of potential zoonotic pathogens in frozen RMBDs that may be a possible source of bacterial infections in pet animals and if transmitted pose a risk for human beings. If non-frozen meat is fed, parasitic infections are also possible. Pet owners should therefore be informed about the risks associated with feeding their animals RMBDs.
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http://dx.doi.org/10.1136/vr.104535DOI Listing
January 2018

Risk ranking of foodborne parasites: State of the art.

Food Waterborne Parasitol 2017 Sep-Dec;8-9:1-13. Epub 2017 Nov 23.

Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.

In a time of increasing threats and decreasing financial resources, monitoring and controlling all possible foodborne hazards at the same time and to the same extent has become more challenging than ever. Therefore, attention is increasingly being paid to the so-called "risk ranking" methods that enable decision makers to focus on the most important foodborne hazards - even when time is limited and knowledge incomplete. In this review paper, we provide an overview of the most common quantitative methods and metrics used for ranking the risks associated with foodborne parasites and present the state of the art on risk ranking exercises for foodborne parasites. A number of risk ranking metrics and methods are available, ranging from simple approaches that can be used to assess the health or economic impact of a foodborne parasitic disease, to more complicated but more comprehensive multi-criteria assessments. For health impact assessment, measures of population health such as disease occurrence and number of deaths; Disability-Adjusted Life Years (DALYs) measuring the healthy life years lost; and Quality-Adjusted Life Years (QALYs) measuring the number of life years lived in optimal health, are described. For economic impact assessment, applied approaches that measure the cost-of-illness from a societal perspective and stated preference methods are outlined. Finally, Multi-Criteria Decision Analysis (MCDA), which can be used to integrate multiple metrics and criteria into a single ranking, is described. These risk ranking methods for foodborne parasites are increasingly performed to aid priority setting at global, regional, and national levels. As different stakeholders have their own prioritization objectives and beliefs, the outcome of such exercises is necessarily context-dependent. Therefore, when designing a risk ranking exercise for foodborne parasites, it is important to choose the metrics and methods, as well as what to rank, in the light of the predefined context of the question being addressed and the target audience.
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http://dx.doi.org/10.1016/j.fawpar.2017.11.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7034010PMC
November 2017

Modelling human Puumala hantavirus infection in relation to bank vole abundance and masting intensity in the Netherlands.

Infect Ecol Epidemiol 2017 24;7(1):1287986. Epub 2017 Mar 24.

Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, The Netherlands.

This paper deals with modelling the relationship between human Puumala hantavirus (PUUV) infection, the abundance and prevalence of infection of the host (the bank vole), mast, and temperature. These data were used to build and parametrise generalised regression models, and parametrise them using datasets on these factors pertaining to the Netherlands. The performance of the models was assessed by considering their predictive power. Models including mast and monthly temperature performed well, and showed that mast intensity influences vole abundance and hence human exposure for the following year. Thus, the model can aid in forecasting of human illness cases, since (1) mast intensity influences the vole abundance and hence human exposure for the following year and (2) monitoring of mast is much more feasible than determining bank vole abundance.
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http://dx.doi.org/10.1080/20008686.2017.1287986DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5443058PMC
March 2017

Immune responses in mice vaccinated with a DNA vaccine expressing serine protease-like protein from the new-born larval stage of Trichinella spiralis.

Parasitology 2017 05 10;144(6):712-719. Epub 2017 Jan 10.

Key Laboratory for Zoonoses Research,Ministry of Education,Institute of Zoonoses,Jilin University,Changchun,People's Republic of China.

Trichinella spiralis is a parasitic helminth that can infect almost all mammals, including humans. Trichinella spiralis infection elicits a typical type 2 immune responses, while suppresses type 1 immune responses, which is in favour of their parasitism. DNA vaccines have been shown to be capable of eliciting balanced CD4+ and CD8+ T cell responses as well as humoral immune responses in small-animal models, which will be advantage to induce protective immune response against helminth infection. In this study, serine protease (Ts-NBLsp) was encoded by a cDNA fragment of new-born T. spiralis larvae, and was inserted after CMV promoter to construct a DNA vaccine [pcDNA3·1(+)-Ts-NBLsp]. Ts-NBLsp expression was demonstrated by immunofluorescence. Sera samples were obtained from vaccinated mice, and they showed strong anti-Ts-NBLsp-specific IgG response. Mice immunized with the pcDNA3·1(+)-Ts-NBLsp DNA vaccine showed a 77·93% reduction in muscle larvae (ML) following challenge with T. spiralis ML. Our results demonstrate that the vaccination with pcDNA3·1(+)-Ts-NBLsp plasmid promoted the balance of type 1 and 2 immune responses and produced a significant protection against T. spiralis infection in mice.
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http://dx.doi.org/10.1017/S0031182016002493DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5426336PMC
May 2017

Marked increase in leptospirosis infections in humans and dogs in the Netherlands, 2014.

Euro Surveill 2016 Apr;21(17)

Centre for Infectious Disease Control (CIb), National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.

In the Netherlands, 97 human leptospirosis cases were notified in 2014. This represents a 4.6-fold increase in autochthonous cases (n = 60) compared with the annual average between 2010 and 2013. Most cases had symptom onset between June and November. This marked increase in humans coincided with an increase of leptospirosis in dogs. In 2014, 13 dogs with leptospirosis were reported, compared with two to six dogs annually from 2010 to 2013. The majority of the autochthonous cases (n = 20) were linked to recreational exposure, e.g. swimming or fishing, followed by occupational exposure (n = 15). About sixty per cent (n = 37) of the autochthonous cases were most likely attributable to surface water contact, and 13 cases to direct contact with animals, mainly rats. A possible explanation for this increase is the preceding mild winter of 2013-2014 followed by the warmest year in three centuries, possibly enabling rodents and Leptospira spp. to survive better. A slight increase in imported leptospirosis was also observed in Dutch tourists (n = 33) most of whom acquired their infection in Thailand (n = 18). More awareness and early recognition of this mainly rodent-borne zoonosis by medical and veterinary specialists is warranted.
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http://dx.doi.org/10.2807/1560-7917.ES.2016.21.17.30211DOI Listing
April 2016

Molecular characterization of human Cryptosporidium spp. isolates after an unusual increase in late summer 2012.

Parasit Vectors 2016 Mar 10;9:138. Epub 2016 Mar 10.

Centre for Infectious Disease Control Netherlands, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands.

Background: During the late summer 2012, a number of medical microbiological laboratories (MMLs) reported an unusual increase in cases of cryptosporidiosis, a gastrointestinal infection caused by the protozoan parasites Cryptosporidium spp. Prompted by this signal, the National Institute of Public Health and the Environment (RIVM) started an epidemiological investigation into possible causes. Simultaneously, samples diagnosed at MMLs were sent to RIVM for genotyping, aiming to further identify the possible source of the increase.

Methods: Genotyping was performed by sequencing a fragment of the GP60 gene. Additional genotyping was performed on a subset of samples using six microsatellite markers. Population genetic analysis was performed using BEAST.

Results: The majority of the samples were typed as C. hominis, and a single GP60 genotype (IbA10G2) largely predominated. Genotyping microsatellite markers further supported the circulation of a single genetic type. Population genetic analysis with genotypes found in previous years is inconsistent with a decrease in effective population size.

Conclusions: The conclusion of this finding is that the rise reflects more an overall increase and not a common source outbreak.
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http://dx.doi.org/10.1186/s13071-016-1397-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4785642PMC
March 2016

Presence of zoonotic agents in engorged ticks and hedgehog faeces from Erinaceus europaeus in (sub) urban areas.

Parasit Vectors 2015 Apr 9;8:210. Epub 2015 Apr 9.

Centre for Zoonoses & Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, the Netherlands.

Background: European hedgehogs (Erinaceus europaeus) are hosts for Ixodes hexagonus and I. ricinus ticks, which are vectors for zoonotic microorganisms. In addition, hedgehogs may carry several enteric zoonoses as well. It is unclear to what extent a presence of pathogens in hedgehogs poses a risk to public health, as information on the presence of zoonotic agents in hedgehogs in urban areas is relatively scarce.

Methods: Engorged ticks and hedgehog faeces were collected from rehabilitating hedgehogs. Ticks were screened individually for presence of Borrelia burgdorferi sensu lato, B. miyamotoi, Anaplasma phagocytophilum, and Candidatus Neoehrlichia mikurensis using PCR-based assays. Faecal samples were screened for presence of Campylobacter, Salmonella, Giardia, Cryptosporidium, and extended-spectrum cephalosporin-resistant-Escherichia coli (ESC)-resistant E. coli, using both culture-based and PCR-based methods.

Results: Anaplasma phagocytophilum and Borrelia genospecies B. afzelii, B. spielmanii, B. garinii, and B. burgdorferi sensu stricto were detected in both I. hexagonus and I. ricinus ticks. Despite their widespread distribution in the Netherlands, B. miyamotoi and Candidatus N. mikurensis were not detected in collected ticks. Analysis of hedgehog faecal samples revealed the presence of Salmonella enterica subspecies enterica and Campylobacter jejuni. In addition, ESC-resistant E. coli were observed in high prevalence in faecal samples, but no Shiga-toxin producing-E.coli were detected. Finally, potentially zoonotic protozoan parasites were observed in hedgehog faecal samples as well, including Giardia duodenalis assemblage A, Cryptosporidium parvum subtypes IIaA17G1R1 and IIcA5G3, and C. hominis subtype IbA10G2.

Conclusions: European hedgehogs in (sub)urban areas harbor a number of zoonotic agents, and therefore may contribute to the spread and transmission of zoonotic diseases. The relatively high prevalence of B. burgdorferi s.l. and A. phagocytophilum in engorged ticks, suggests that hedgehogs contribute to their enzootic cycles in (sub)urban areas. To what extent can hedgehogs maintain the enteric zoonotic agents in natural cycles, and the role of (spill-back from) humans remains to be investigated.
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http://dx.doi.org/10.1186/s13071-015-0814-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4406014PMC
April 2015

Intervention strategies to reduce human Toxoplasma gondii disease burden.

Clin Infect Dis 2015 Jan 15;60(1):101-7. Epub 2014 Sep 15.

Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven.

Infection with Toxoplasma gondii is acquired through consumption of undercooked infected meat, or by uptake of cat-shed oocysts. Although congenital toxoplasmosis is generally considered to contribute most to the disease burden of T. gondii, ocular disease from acquired infection was recently shown to add substantially to the burden. In addition, toxoplasmosis in immune-compromised individuals usually results from reactivation of an infection acquired earlier in life. Nevertheless, prevention of toxoplasmosis commonly targets mainly pregnant women. We summarize current prevention strategies of congenital toxoplasmosis and evaluate options to improve protection of the general population (including pregnant women). To protect the general population, freezing of meat destined for raw or undercooked consumption is the most readily applicable option, especially when limited to meat from animals originating from nonbiosecure husbandry systems. In the long term, more health benefits are expected from cat vaccination; therefore, development of a cat vaccine and evaluation of its implementation is a research priority.
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http://dx.doi.org/10.1093/cid/ciu721DOI Listing
January 2015

An experimental Toxoplasma gondii dose response challenge model to study therapeutic or vaccine efficacy in cats.

PLoS One 2014 3;9(9):e104740. Epub 2014 Sep 3.

Central Veterinary Institute of Wageningen UR, Department of Infection Biology, Lelystad, The Netherlands.

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.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0104740PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4153576PMC
May 2015

Response to Galán-Puchades and Fuentes: Taenia asiatica: neglected--but not forgotten--and almost certainly being quietly globalised.

Trends Parasitol 2014 Feb 16;30(2):56-7. Epub 2014 Jan 16.

United States Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USA.

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http://dx.doi.org/10.1016/j.pt.2013.12.008DOI Listing
February 2014

Impacts of globalisation on foodborne parasites.

Trends Parasitol 2014 Jan 17;30(1):37-52. Epub 2013 Oct 17.

United States Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705 USA.

Globalisation is a manmade phenomenon encompassing the spread and movement of everything, animate and inanimate, material and intangible, around the planet. The intentions of globalisation may be worthy--but may also have unintended consequences. Pathogens may also be spread, enabling their establishment in new niches and exposing new human and animal populations to infection. The plethora of foodborne parasites that could be distributed by globalisation has only recently been acknowledged and will provide challenges for clinicians, veterinarians, diagnosticians, and everyone concerned with food safety. Globalisation may also provide the resources to overcome some of these challenges. It will facilitate sharing of methods and approaches, and establishment of systems and databases that enable control of parasites entering the global food chain.
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http://dx.doi.org/10.1016/j.pt.2013.09.005DOI Listing
January 2014

A prospective study among patients presenting at the general practitioner with a tick bite or erythema migrans in The Netherlands.

PLoS One 2013 16;8(5):e64361. Epub 2013 May 16.

Epidemiology and surveillance unit, Centre for Infectious Disease Control Netherlands, National Institute for Public Health and the Environment, Bilthoven, The Netherlands.

Background: We performed a nationwide prospective study on the transmission risk for Borrelia to humans, investigating symptoms and serology at enrolment and three months after tick bites, and after standard treatment for erythema migrans (EM). Aiming to quantify the infection risk at point of care by physicians, we explored risk factors such as tick testing for Borrelia and assessment of the duration of the tick's blood meal.

Methods And Findings: Questionnaires, blood samples and ticks from patients who consulted one of 307 general practitioners for tick bites (n = 327) or EM (n = 283) in 2007 and 2008, were collected at enrolment and three months later at follow-up. Borrelia burgdorferi sensu lato DNA was detected in 29.3% of 314 ticks, using PCR/reverse line blot and real-time PCR on the OspA gene. Seroconversion in C6 ELISA, IgM or IgG immunoblots for Borrelia-specific antibodies was observed in 3.2% of tick bite cases. Fourteen tick bite cases had evidence of early Borrelia infection, of which EM developed among seven cases. The risk of developing EM after tick bites was 2.6% (95%CI: 1.1%-5.0%), and the risk of either EM or seroconversion was 5.1% (95%CI: 2.9%-8.2%). Participants with Borrelia-positive ticks had a significantly higher risk of either EM or seroconversion (odds ratio 4.8, 95%CI: 1.1-20.4), and of seroconversion alone (odds ratio 11.1, 95%CI: 1.1-108.9). A third (34%) of the cases enrolled with EM did not recall preceding tick bites. Three EM cases (1%) reported persisting symptoms, three months after standard antibiotic treatment for EM.

Conclusions: One out of forty participants developed EM within three months after tick bites. The infection risk can be assessed by tick testing for Borrelia at point of care by physicians. However, further refining is needed considering sensitivity and specificity of tick tests, accuracy of tick attachment time and engorgement.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0064361PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3655959PMC
December 2013

Geodemographic analysis of Borrelia burgdorferi sensu lato using the 5S-23S rDNA spacer region.

Infect Genet Evol 2013 Jul 16;17:216-22. Epub 2013 Apr 16.

Centre for Infectious Disease Control Netherlands, National Institute for Public Health and Environment, RIVM, PO Box 1, 3720 BA Bilthoven, The 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.
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http://dx.doi.org/10.1016/j.meegid.2013.04.009DOI Listing
July 2013

Antibody response against Trichinella spiralis in experimentally infected rats is dose dependent.

Vet Res 2011 Nov 30;42:113. Epub 2011 Nov 30.

Laboratory for Zoonoses and Environmental Microbiology, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands.

Domestic pigs are the main representatives of the domestic cycle of Trichinella spiralis that play a role in transmission to humans. In Europe, backyard pigs of small household farms are the most important risks for humans to obtain trichinellosis. Rats might play a role in the transmission of Trichinella spiralis from domestic to sylvatic animals and vice versa. In order to be able to investigate the role of wild rats in the epidemiology of T. spiralis in The Netherlands, we studied the dynamics of antibody response after T. spiralis infections in experimental rats, using infection doses ranging from very low (10 muscle larvae, ML, per rat) to very high (16,000 ML per rat). To evaluate the feasibility of rats surviving high infection doses with T. spiralis, clinical and pathological parameters were quantified. Serological tools for detecting T. spiralis in rats were developed to quantitatively study the correlation between parasite load and immunological response. The results show that an infection dose-dependent antibody response was developed in rats after infection with as low as 10 ML up to a level of 10,000 ML. A positive correlation was found between the number of recovered ML and serum antibody levels, although specific measured antibody levels correspond to a wide range of LPG values. Serum antibodies of rats that were infected even with 10 or 25 ML could readily be detected by use of the T. spiralis western blot 2 weeks post infection. We conclude that based on these low infection doses, serologic tests are a useful tool to survey T. spiralis in wild rats.
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http://dx.doi.org/10.1186/1297-9716-42-113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3247182PMC
November 2011

Small risk of developing symptomatic tick-borne diseases following a tick bite in The Netherlands.

Parasit Vectors 2011 Feb 10;4:17. Epub 2011 Feb 10.

Laboratory for Zoonoses and Environmental Microbiology, Centre for Infectious Disease Control Netherlands, National Institute for Public Health and Environment (RIVM), Bilthoven, The Netherlands.

Background: In The Netherlands, the incidence of Lyme borreliosis is on the rise. Besides its causative agent, Borrelia burgdorferi s.l., other potential pathogens like Rickettsia, Babesia and Ehrlichia species are present in Ixodes ricinus ticks. The risk of disease associated with these microorganisms after tick-bites remains, however, largely unclear. A prospective study was performed to investigate how many persons with tick-bites develop localized or systemic symptoms and whether these are associated with tick-borne microorganisms.

Results: In total, 297 Ixodes ricinus ticks were collected from 246 study participants who consulted a general practitioner on the island of Ameland for tick bites. Ticks were subjected to PCR to detect DNA of Borrelia burgdorferi s.l., Rickettsia spp., Babesia spp. or Ehrlichia/Anaplasma spp.. Sixteen percent of the collected ticks were positive for Borrelia burgdorferi s.l., 19% for Rickettsia spp., 12% for Ehrlichia/Anaplasma spp. and 10% for Babesia spp.. At least six months after the tick bite, study participants were interviewed on symptoms by means of a standard questionnaire. 14 out of 193 participants (8.3%) reported reddening at the bite site and 6 participants (4.1%) reported systemic symptoms. No association between symptoms and tick-borne microorganisms was found. Attachment duration ≥24 h was positively associated with reddening at the bite site and systemic symptoms. Using logistic regression techniques, reddening was positively correlated with presence of Borrelia afzelii, and having 'any symptoms' was positively associated with attachment duration.

Conclusion: The risk of contracting acute Lyme borreliosis, rickettsiosis, babesiosis or ehrlichiosis from a single tick bite was <1% in this study population.
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http://dx.doi.org/10.1186/1756-3305-4-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3050846PMC
February 2011

Identification of zoonotic genotypes of Giardia duodenalis.

PLoS Negl Trop Dis 2009 Dec 1;3(12):e558. Epub 2009 Dec 1.

Laboratory for Zoonoses and Environmental Microbiology, National Institute for Public Health and Environment (RIVM), Bilthoven, The Netherlands.

Giardia duodenalis, originally regarded as a commensal organism, is the etiologic agent of giardiasis, a gastrointestinal disease of humans and animals. Giardiasis causes major public and veterinary health concerns worldwide. Transmission is either direct, through the faecal-oral route, or indirect, through ingestion of contaminated water or food. Genetic characterization of G. duodenalis isolates has revealed the existence of seven groups (assemblages A to G) which differ in their host distribution. Assemblages A and B are found in humans and in many other mammals, but the role of animals in the epidemiology of human infection is still unclear, despite the fact that the zoonotic potential of Giardia was recognised by the WHO some 30 years ago. Here, we performed an extensive genetic characterization of 978 human and 1440 animal isolates, which together comprise 3886 sequences from 4 genetic loci. The data were assembled into a molecular epidemiological database developed by a European network of public and veterinary health Institutions. Genotyping was performed at different levels of resolution (single and multiple loci on the same dataset). The zoonotic potential of both assemblages A and B is evident when studied at the level of assemblages, sub-assemblages, and even at each single locus. However, when genotypes are defined using a multi-locus sequence typing scheme, only 2 multi-locus genotypes (MLG) of assemblage A and none of assemblage B appear to have a zoonotic potential. Surprisingly, mixtures of genotypes in individual isolates were repeatedly observed. Possible explanations are the uptake of genetically different Giardia cysts by a host, or subsequent infection of an already infected host, likely without overt symptoms, with a different Giardia species, which may cause disease. Other explanations for mixed genotypes, particularly for assemblage B, are substantial allelic sequence heterogeneity and/or genetic recombination. Although the zoonotic potential of G. duodenalis is evident, evidence on the contribution and frequency is (still) lacking. This newly developed molecular database has the potential to tackle intricate epidemiological questions concerning protozoan diseases.
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http://dx.doi.org/10.1371/journal.pntd.0000558DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2777335PMC
December 2009

Persistent detection of Babesia EU1 and Babesia microti in Ixodes ricinus in the Netherlands during a 5-year surveillance: 2003-2007.

Vector Borne Zoonotic Dis 2009 Feb 30;9(1):119-22. Epub 2008 Aug 30.

National Institute for Public Health and the Environment, the Netherlands.

We report the finding of Babesia EU1 and Babesia microti in Ixodes ricinus ticks in the Netherlands. During 5 years of surveillance between 2003 and 2007, 1488 ticks were collected in a dune forest area near the North Sea and were screened for Babesia infections. In 17 ticks, DNA of the protozoan parasite genus Babesia was detected using a Babesia-specific 18S rRNA polymerase chain reaction. Further, reverse line blot analysis and DNA sequence analysis showed that 13 of these ticks carried Babesia EU1, two ticks carried B. microti, and one tick carried B. divergens. This study shows that the human pathogenic species Babesia EU1 and B. microti can complete their life cycle in the Netherlands.
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http://dx.doi.org/10.1089/vbz.2008.0047DOI Listing
February 2009

Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands.

Int J Parasitol 2008 Jun 4;38(7):809-17. Epub 2007 Nov 4.

National Institute for Public Health and the Environment (RIVM), Centre for Infectious Disease Control (Cib), Laboratory for Zoonoses and Environmental Microbiology (LZO), Antonie van Leeuwenhoeklaan 9, Bilthoven, The Netherlands.

The protozoan parasite Cryptosporidium is found world-wide and can cause disease in both humans and animals. To study the zoonotic potential of Cryptosporidium in The Netherlands we isolated this parasite from the faeces of infected humans and cattle and genotyped those isolates for several different markers. The overall genotyping results showed: for humans isolates, 70% Cryptosporidium hominis, 19% Cryptosporidium parvum, 10% a combination of C. hominis and C. parvum, and 1% Cryptosporidium felis; and for cattle isolates 100% C. parvum. Analysis of the genetic variants detected for the HSP70, ML1 and GP60 markers showed: for human isolates, one C. hominis and two C. parvum variants (C. parvum and C. parvum NL) for HSP70, one C. hominis and five C. parvum variants (C1, C2, C3, and C2 NL1 and C2 NL2) for ML1, four C. hominis (mainly IbA10G2) and four C. parvum variants (mainly IIaA15G2R1) for GP60; and the cattle isolates only C. parvum (not C. parvum NL1) for HSP70, C1 and C2 for ML1, and 17 different IIa sub-types (mainly IIaA15G2R1) for GP60. Molecular epidemiological analysis of the human data showed a C. hominis peak in autumn. The majority (80%) of the human cases were children aged between 0 and 9 years and >70% of these were caused by C. hominis. Patients >25 years of age were infected mainly with C. parvum. We conclude that C. hominis IbA10G2 is found at high frequencies in autumn in humans and not in cattle. The high prevalence of C. parvum IIaA15G2R1 in both humans and cattle indicates that cattle may be a reservoir for this sub-type in The Netherlands.
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http://dx.doi.org/10.1016/j.ijpara.2007.10.014DOI Listing
June 2008

Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands.

Appl Environ Microbiol 2006 Dec 6;72(12):7594-601. Epub 2006 Oct 6.

Microbiological Laboratory for Health Protection, National Institute for Public Health and the Environment, Antonie van Leeuwenhoeklaan 9, Bilthoven 3720 BA, The Netherlands.

From 2000 to 2004, ticks were collected by dragging a blanket in four habitat areas in The Netherlands: dunes, heather, forest, and a city park. Tick densities were calculated, and infection with Borrelia burgdorferi and Anaplasma and Ehrlichia species was investigated by reverse line blot analysis. The lowest tick density was observed in the heather area (1 to 8/100 m2). In the oak forest and city park, the tick densities ranged from 26 to 45/100 m2. The highest tick density was found in the dune area (139 to 551/100 m2). The infection rates varied significantly for the four study areas and years, ranging from 0.8 to 11. 5% for Borrelia spp. and 1 to 16% for Ehrlichia or Anaplasma (Ehrlichia/Anaplasma) spp. Borrelia infection rates were highest in the dunes, followed by the forest, the city park, and heather area. In contrast, Ehrlichia/Anaplasma was found most often in the forest and less often in the city park. The following Borrelia species were found: Borrelia sensu lato strains not identified to the species level (2.5%), B. afzelii (2.5%), B. valaisiana (0.9%), B. burgdorferi sensu stricto (0.13%), and B. garinii (0.13%). For Ehrlichia/Anaplasma species, Ehrlichia and Anaplasma spp. not identified to the species level (2.5%), Anaplasma schotti variant (3.5%), Anaplasma phagocytophilum variant (0.3%), and Ehrlichia canis (0.19%) were found. E. canis is reported for the first time in ticks in The Netherlands in this study. Borrelia lusitaniae, Ehrlichia chaffeensis, and the human granylocytic anaplasmosis agent were not detected. About 1.6% of the ticks were infected with both Borrelia and Ehrlichia/Anaplasma, which was higher than the frequency predicted from the individual infection rates, suggesting hosts with multiple infections or a possible selective advantage of coinfection.
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http://dx.doi.org/10.1128/AEM.01851-06DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1694262PMC
December 2006

Base line prevalence and spatial distribution of Echinococcus multilocularis in a newly recognized endemic area in the Netherlands.

Vet Parasitol 2004 Jan;119(1):27-35

Microbiological Laboratory for Health Protection, National Institute for Public Health and the Environment, Antonie van Leeuwenhoeklaan 9, P.O. Box 1, 3720 BA Bilthoven, The Netherlands.

The base line prevalence of Echinococcus multilocularis in foxes was determined in the eastern part of the province of Groningen in the Netherlands adjacent to the German border. This region has been identified in a previous study in 1998 as one of the westernmost border areas of E. multilocularis. Base line prevalence data are important for a better insight in the possible spread of the parasite and its changes in time. As fox feces containing E. multilocularis eggs are an important source for human exposure this base line prevalence is also an indicator for the potential risk for public health. The base line prevalence was estimated at 9.4% (95% CI: 5.2-16.5%). These results confirm previous findings of E. multilocularis in the same region. The spatial distribution of the infected foxes has been analyzed as a spatial gradient using a logistic model. The prevalence appeared to change strongest in east-western direction and was highest near the German border, adjacent to a German endemic area. These results suggest that the border areas in the Netherlands are the most margin of E. multilocularis territory.
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http://dx.doi.org/10.1016/j.vetpar.2003.11.001DOI Listing
January 2004
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