We investigated Estonian population and its selected subgroups for serological evidence of exposure to Ascaris lumbricoides, Echinococcus spp., Taenia solium, Toxocara canis, Toxoplasma gondii, and Trichinella spiralis. Serum samples from 999 adults representing general population, 248 children aged 14–18, 158 veterinarians, 375 animal caretakers, and 144 hunters were tested for specific immunoglobulin G antibodies against the selected parasites using commercial enzyme immunoassays (ELISA). Sera yielding positive or twice grey zone Echinococcus spp, T. solium, T. canis, and T. spiralis results were subjected to western blot (WB) analysis. In the general population, based on the ELISA results, the A. lumbricoides seroprevalence was 12.7%, Echinococcus spp. seroprevalence was 3.3%, T. solium seroprevalence was 0.7%, T. canis seroprevalence was 12.1%, T. gondii seroprevalence was 55.8%, and T. spiralis seroprevalence was 3.1%. Ascaris lumbricoides seroprevalences were higher in children and in animal caretakers than in the general population, and T. canis seroprevalence was higher in animal caretakers than in the general population. Compared with the general population, Echinococcus spp. seroprevalence was higher in children. By contrast, T. gondii seroprevalence was higher in animal caretakers, and lower in children, than in the general population. In the general population, the WB-confirmed Echinococcus spp. seroprevalence was 0.5%, T. solium cysticercosis seroprevalence was 0.0%, Toxocara spp. seroprevalence was 14.5%, and Trichinella spp. seroprevalence was 2.7%. WB-confirmed Toxocara spp. seroprevalence was higher in animal caretakers than in the general population. We found serological evidence of exposure to zoonotic parasites in all tested groups. This calls for higher awareness of zoonotic parasitic infections in Estonia.
Citation: Lassen B, Janson M, Viltrop A, Neare K, Hütt P, Golovljova I, et al. (2016) Serological Evidence of Exposure to Globally Relevant Zoonotic Parasites in the Estonian Population. PLoS ONE 11(10): e0164142. https://doi.org/10.1371/journal.pone.0164142
Editor: Emmanuel Serrano Ferron, Universidade de Aveiro, PORTUGAL
Received: March 30, 2016; Accepted: September 20, 2016; Published: October 10, 2016
Copyright: © 2016 Lassen et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data can be found within the paper.
Funding: The study was supported by the Health Board of Estonia, the European Regional Development Fund programme TerVe 3.2.1002.11. project EKZE-SS, project funding M14143VLVP from the Strategic Development Fund of the Estonian University of Life Sciences, the Estonian Science Foundation grant ETF9433, and Base Financing of Estonian University of Life Sciences, project funding 8P160014VLVP. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Comprehensive studies on exposure to zoonotic parasites are needed [1, 2]. Zoonoses present a challenge to public health and wealth, and some groups, such as children and immunocompromised persons, are more vulnerable [3, 4]. Zoonotic infections can also be an occupational risk for groups including veterinarians, animal caretakers, and hunters [5, 6, 7, 8, 9].
Recent research confirms that several zoonotic parasites are common and endemic in Estonia, which is located in north-eastern Europe [10, 11, 12, 13, 14, 15, 16, 17]. We designed a cross-sectional serological study to investigate the exposure to Ascaris spp., Echinococcus spp., Taenia solium, Toxocara canis, Toxoplasma gondii, and Trichinella spiralis in the Estonian population and its four subgroups: children aged 14–18, animal caretakers, hunters, and veterinarians.
The selected parasites are ranked high among zoonotic parasites that were evaluated for their global relevance as foodborne pathogens [1, 2]: T. solium as the 1st, E. granulosus 2nd, E. multilocularis 3rd, T. gondii 4th, T. spiralis 7th, Ascaris spp. 9th, Trichinella spp. 16th and Toxocara spp. 20th .
Echinococcus spp. are endemic in the Baltic countries, and the incidence of human cases has increased . This is in conflict with the statement that the risk of acquiring echinococcosis in Estonia would be negligible . Until 2014, official reports mention 13 cases of human echinococcosis, four of which were classified as imported .
There are no available reports of human infections with Toxocara spp. from Estonia.
The highest reported incidence of T. solium infections was 14.8 per 100000 inhabitants in 1959 . Official Estonian public health information mentions two human T. solium infections from 2000–2001 .
The local T. gondii seroprevalence has been high: in the town of Tartu, 61.8% in 1991–1993  and 54.9% in 1999–2001 . Seropositivity indicates chronic infection with the parasite. Since 1999, 78 cases of toxoplasmosis have been reported in Estonia [20, 21, 22], including three cases of congenital toxoplasmosis: two from 2002 and one from 2003 (1.54 and 0.77 per 10000 births, respectively).
In this nationwide study, we aimed to estimate the seroprevalences of the selected zoonotic parasites, and to evaluate the differences in seroprevalence between the general population and the subgroups. Our hypothesis was that people in Estonia would have serological evidence of exposure to all of the parasites, and that in certain subgroups, the seroprevalences would be higher compared to general population.
Material and Methods
The study was approved by the Research Ethics Committee of the University of Tartu (nr. 216/T-15, 227/M-5 and 235/M-26).
The general population samples were obtained from a biobank (http://www.geenivaramu.ee/en) and the children samples were obtained from a sample collection (National Institute for Health Development, http://tai.ee/en/). There had been no formal signed informed consent of a parent or guardian of the children, but written information had been given and it had been emphasized that the participation was voluntary. The veterinarians, animal caretakers, and hunters gave written informed consent before the blood samples were taken by nurses. The sera were stored and analysed coded.
Those veterinarians, animal caretakers, and hunters who had provided contact information were informed of their serology results and given a short description of what seropositivity means. In addition, they were provided the contact information for designated research group members, to whom further questions could be addressed. Those with medical questions were guided to consult their own family physician.
Estonia is located in the north-eastern Europe and has a population of 1.3 million inhabitants . Approximately 1000 veterinary practitioners are licenced to work in the country . The number of persons working as animal caretakers is unknown. There are over 15000 hunters .
The general population samples (n = 999), from individuals 18 years and older, were obtained as a random sample stratified by county and gender from the serum bank of the Estonian Genome Center. The samples had been collected in 2004–2011.
Sera from apparently healthy children aged 14–18 years (n = 248) were obtained from a serum bank that had been collected in 2003. The samples originated from different parts of the country.
Veterinarians (n = 158) were sampled at a local veterinary conference in October 2012.
Animal caretakers (n = 375) included persons involved with dairy cattle (n = 193), beef cattle (n = 51), pigs (n = 68), and sheep and goats (n = 63). From those involved with dairy cattle, blood samples were collected in March–May 2013, whereas those involved with beef cattle were sampled in January 2014. Animal caretakers involved with pigs were sampled in September–November 2013, and those involved with sheep and goats were sampled in October–November 2013. Those involved with pigs were sampled during farm visits, whereas the collection of the other samples was arranged at local professional meetings and events.
Hunters (n = 144) were sampled during a national meeting of hunters in July 2013.
General population samples and children samples were stored frozen at -20°C and thawed prior to the analyses. The samples from veterinarians, animal caretakers, and hunters were allowed to clot and then centrifuged, at the sampling site. The sera were separated within 24 hours. The sera were stored at +4°C for up to two days, during which the first analyses were performed, and then frozen at -20°C until thawed prior to further analyses.
The serum samples were tested using NovaLisa IgG enzyme immunoassays (ELISA) (NovaTec Immunodiagnostica GmbH, Dietzenbach, Germany) for the presence of immunoglobulin G (IgG) antibodies against A. lumbricoides (specificity (Sp) 95%), sensitivity (Se) >95%), Echinococcus spp. (Sp >95%, Se >95%), T. solium (Sp >95%, Se 93.8%), T. gondii (Sp 98.2%, Se 96.6%), T. canis (Sp >95%, Se >95%), and T. spiralis (Sp 94.8%, Se >95%), according to the manufacturer’s instructions. The controls provided in the kits were used in each analysis. They included standards A, B, C, and D for the T. gondii ELISA, and positive control, cut-off control, and negative control for the other ELISAs.
The samples that tested positive with ELISA were considered seropositive. The samples that yielded a grey zone result were retested, and the second test result was considered the final ELISA result.
Samples that had tested positive or yielded a grey zone result twice with the Echinococcus spp., T. solium, T. canis and T. spiralis ELISA were further tested using ECHINOCOCCUS Western Blot IgG, CYSTICERCOSIS Western Blot IgG, TOXOCARA Western Blot IgG, and TRICHINELLA Western Blot IgG (LDBIO DIAGNOSTICS, Lyon, France), respectively. The positive controls provided in the kits were used in each analysis. The results were interpreted following the manufacturer’s instructions.
The samples that tested positive with the western blot (WB) were considered confirmed seropositives. It is noteworthy that the T. solium ELISA is intended for detecting antibodies against T. solium antigens, both taeniasis and cysticercosis, while the corresponding WB is based on antigens from crude larval extract and intended for detecting cysticercosis caused by the larval stages of the parasite only.
The crude seroprevalences were calculated using the number of seropositives (ELISA result) as the numerator. The WB-confirmed seroprevalences were calculated using the number of confirmed seropositives (ELISA and WB in series) as the numerator. The true seroprevalences (Rogan-Gladen) were calculated using the number of seropositives (ELISA result) and taken into account the Sp and Se, with EpiTools . If the Sp or Se was given as “>95%”, the calculation was done using 95%. The denominator was the number of samples tested in each group.
Exclusion of samples
The database was searched for double entries: one sample from general population and one sample from animal caretakers (persons involved with beef cattle) were excluded.
The statistical analyses were performed using the free software OpenEpi . Confidence intervals (95% CI) were calculated using Mid-P exact test. Two-by-two tables were used to evaluate differences in crude seroprevalences between the groups. Bonferroni adjustment was used to reduce the likelihood of type 1 error, and differences with two-tailed p-values < 0.01 (Mid-P exact test) were considered statistically significant. When comparing a single result of ours to another published result, a difference with two-tailed p-value < 0.05 (Mid-P exact test) was considered statistically significant.
The A. lumbricoides seroprevalence was 12.7% in the general population. All groups showed evidence of exposure to A. lumbricoides (Table 1). The seroprevalence was significantly higher in children and in animal caretakers than in the general population (p < 0.001).
The true A. lumbricoides seroprevalence was 8.6% (95% CI 6.3–10.9) in the general population, 29.4% (95% CI 23.0–35.8) in children, 4.3% (95% CI -0.6–9.2) in veterinarians, 18.4% (95% CI 13.8–23.1) in animal caretakers, and 9.9% (95% CI 3.6–16.2) in hunters.
The Echinococcus spp. seroprevalence was 3.3% and the WB-confirmed Echinococcus spp. seroprevalence was 0.5% in the general population. All groups showed evidence of exposure to Echinococcus spp. (Table 2). The seroprevalence was higher in children (p < 0.001) than in the general population. WB-confirmed seropositives were detected in the general population and animal careretakers group.
The true Echinococcus spp. seroprevalence was <0% (95% CI -3.1-(-0.7)) in the general population, 7.9% (95% CI 3.4–12.4) in children, <0% (95% CI -5.8-(-1.1)) in veterinarians, <0% (95% CI -5.5-(-3.2)) in animal caretakers, and <0% (95% CI -6.3-(-3.3)) in hunters.
The T. solium seroprevalence was 0.7% and the WB-confirmed T. solium cysticercosis seroprevalence was 0.0% in the general population. Seropositive individuals were detected in all groups except the children (Table 3).
The true T. solium seroprevalence was <0% (95% CI -6.8-(-5.6)) in the general population, <0% (95% CI -7.0-(-7.0)) in children, <0% (95% CI -7.7-(-4.9)) in veterinarians, <0% (95% CI -7.1-(-5.1)) in animal caretakers, and <0% (95% CI -7.6-(-3.3)) in hunters.
The T. canis seroprevalence was 12.1% and the WB-confirmed Toxocara spp. seroprevalence was 14.5% in the general population. All groups showed evidence of exposure to T. canis (Table 4). The seroprevalence was higher in animal caretakers (p < 0.001) than in the general population. The WB-confirmed Toxocara spp. seroprevalence was also higher in animal caretakers (p < 0.001) than in the general population.
The true T. canis seroprevalence was 7.9% (95% CI 5.7–10.2) in the general population, 13.3% (95% CI 8.1–18.4) in children, 2.9% (95% CI -1.7–7.5) in veterinarians, 23.2% (95% CI 18.3–28.1) in animal caretakers, and 10.6% (95% CI 4.2–17.1) in hunters.
The T. gondii seroprevalence was 55.8% in the general population. All groups showed evidence of exposure to T. gondii (Table 5). The seroprevalence was higher in animal caretakers (p < 0.01), and lower in children (p < 0.001), than in the general population.
The true T. gondii seroprevalence was 55.2% (95% CI 52.0–58.5) in the general population, 36.0% (95% CI 29.6–42.3) in children, 45.2% (95% CI 37.0–53.4) in veterinarians, 74.9% (95% CI 70.2–79.6) in animal caretakers, and 65.3% (95% CI 57.1–73.5) in hunters.
The T. spiralis seroprevalence was 3.1% and the WB-confirmed Trichinella spp. seroprevalence was 2.7% in the general population. All groups showed evidence of exposure to T. spiralis (Table 6).
The true T. spiralis seroprevalence was <0% (95% CI -3.3-(-0.9)) in the general population, <0% (95% CI -4.4–0.5) in children, <0% (95% CI -5.1–0.1) in veterinarians, <0% (95% CI -3.8–0.4) in animal caretakers, and 0.6% (95% CI -3.5–4.8) in hunters.
We detected evidence of exposure to all of the zoonotic parasites tested. These zoonotic parasites present a threat to human health and life quality, animal health and welfare, food safety, the economy, and the environment [1, 32, 33]. The results of this study call for higher awareness of zoonotic parasitic infections in Estonia.
The A. lumbricoides seroprevalence in general population was lower than an estimate from the Netherlands (33.0%, p < 0.001) . The A. lumbricoides seroprevalence estimate in children in Estonia was higher than estimates from Poland (15.0%, p < 0.001)  and from the Netherlands (7.2%, p < 0.001) . In our study, the seroprevalence was higher in the children than in adults. This is in contrast to an increase in seroprevalence with age that was observed in the Netherlands . One possible explanation could be that exposure to this parasite would have increased recently in Estonia, but there are no direct data to support that. The higher seroprevalence in animal caretakers might be due to contact with Ascaris eggs in the agricultural environment.
The Echinococcus spp. seroprevalence estimate in general population was higher than that observed in Austria (0.0%, p < 0.001)  and Greece (1.1%, p < 0.01) , but similar to that observed in Poland (3.2%)  and Spain (3.4%) . The seroprevalence in veterinarians was similar to that in veterinary surgeons in Turkey (2.2%) . The Echinococcus spp. seroprevalence in hunters was lower than both E. granulosus seroprevalence (10.7%, p < 0.001) and E. multilocularis seroprevalence (5.4%, p < 0.05) in hunters in Austria , while none of the seropositives in either of the studies tested positive with WB. The data available on Echinococcus spp. infections in animal hosts originates mainly from research projects, but E. multilocularis, E. canadensis (G8 and G10) of E. granulosus (G1) have been diagnosed in animal hosts in Estonia recently .
The T. canis seroprevalence in general population was higher than the estimates from Austria (6.3%, p < 0.001) , Sweden (7.1%, p < 0.01) , Denmark (2.6%, p < 0.001) , and the Netherlands (8.3%, p < 0.001) , but similar to that from Poland (13.0%)  and that from the Slovak Republic 20 years ago (13.7%) . The WB-confirmed Toxocara spp. seroprevalence was higher than a similarly confirmed estimate from Denmark (2.4%, p < 0.001)  and higher than people with epilepsy in Italy when tested with a comparable method (6.5%, p < 0.01) . The T. canis seroprevalence and the WB-confirmed Toxocara spp. seroprevalence in hunters were similar to those in hunters in Austria (16.8%) –in both studies, all seropositive hunters tested positive also with WB. The WB-confirmed Toxocara spp. seroprevalence in children was higher than a similarly confirmed estimate from children from Poland (4.2%, p < 0.001) . Toxocara spp. are endemic in animal hosts in Estonia [50, 51, 52], and Toxocara spp. eggs have been found shed into the urban environment [51, 52].
The T. gondii seroprevalences were worryingly high when compared with recent results from other European countries, where the seroprevalence has decreased [53, 54]. The burden caused by T. gondii infections is high [1, 2, 32] and the parasite merits attention. Toxoplasma gondii seroprevalence typically increases with age, indicating acquired infections. The high T. gondii seroprevalence in children in Estonia suggests that the infection pressure is substantial, while different age distribution might partly explain some of the differences noted between other groups. Contact with contaminated environment on farms  may partly explain the higher seroprevalence in farm workers. High T. gondii seroprevalence in domestic cats in Estonia  indicates that the environment has been contaminated with oocysts, which is supported by results from wild and domestic animals [12, 16].
The T. spiralis seroprevalence in the general population was similar to an estimate in forest workers in Poland (6.0%) , and the WB-confirmed Trichinella spp. seroprevalence was similar to an estimate in hunting communities in Greenland (3.3%) . Trichinella spp. merit higher awareness as relevant zoonotic parasites in Estonia, in animal hosts particularly in the sylvatic cycle .
The sample sizes were adequate for estimating and comparing the seroprevalences. The general population samples were a good representation of the Estonian population. The children group only included samples from youngsters aged over 14 years; thus the seroprevalences in younger children remain unknown. The convenience samples from children, veterinarians, animal caretakers, and hunters may be limited by geographical representativeness; those interested in research activities and further professional education may be overrepresented.
Serology is an indirect detection method. For detecting chronic T. gondii infections, serology is widely used, whereas for other parasites, serology results should be interpreted with more caution. Detecting antibodies provides evidence of exposure and can indicate infection  and has been used in follow-up of patients. For example, patients with alveolar echinococcosis appear to maintain ELISA-seropositivity despite the intensity of the WB bands may fade during the follow-up, while a curative resection results in seronegativity in some patients in a few years .
We chose to investigate the presence of IgG antibodies because they are commonly long-lasting and suitable for epidemiological studies. However, investigating only one class of antibodies is a limitation of the study.
The assays used are based on purified antigens, but some potential cross-reactions are listed by the manufacturer. Of the 499 T. canis positive samples, 130 (26.1%) tested positive for antibodies against A. lumbricoides and ten (2.0%) tested positive for antibodies against Echinococcus spp. with the corresponding ELISA assays. A majority (99.1%) of T. canis results tested positive with the corresponding WB. One sample that had tested positive for antibodies against T. canis and for antibodies against Echinococcus spp. tested positive for both with the corresponding WB assays.
Overall, it appeared to be a good decision to include also samples that yielded a grey zone ELISA result twice to be tested with WB. Several samples yielded a grey zone result twice with ELISA but tested positive with WB (Tables 2, 4 and 6).
The methods were evaluated to be suitable for an epidemiological study, although communicating an individual result required explaining the main limitations of the methods used. Informing the veterinarians, animal caretakers, and hunters of their results was evaluated to be an ethically reasoned choice.
These results provide baseline data, which can inform public health decision makers and suggest where further research and prevention efforts should be targeted. It is obvious that the zoonotic parasites circulating in Estonia reach also humans, but the locally relevant risk factors for encountering the parasites are currently largely unknown.
People living in Estonia had evidence of having been exposed to several zoonotic parasites, which calls for evaluation of need of prevention strategies and higher awareness. Antibodies against zoonotic parasites appeared to be formed already in childhood, indicating considerable infection pressure. The results suggest that zoonotic parasitic infections are underdiagnosed or underreported in Estonia.
The authors thank Pille Paats for technical assistance, nurses Anu Kuusmann and Marge Reiss for collecting blood samples, Jevgenia Epštein for providing national health data, and Irina Reshetnjak and the late Valentina Tefanova for contributing to the collection of children sera. The general population samples and associated information were provided by the Estonian Genome Center, University of Tartu (The Estonian Biobank).
- Conceptualization: PJ BL AV.
- Data curation: MJ BL.
- Formal analysis: BL PJ AV.
- Funding acquisition: AV BL PJ.
- Investigation: MJ KN BL LT.
- Methodology: BL AV PJ PH MJ KN.
- Project administration: AV BL IG.
- Resources: IG.
- Supervision: BL AV LT.
- Validation: BL MJ.
- Visualization: BL.
- Writing – original draft: BL PJ MJ.
- Writing – review & editing: BL PJ MJ AV PH KN IG LT.
- 1. Food and Agriculture Organization of the United Nations/World Health Organization. Multicriteria-based ranking for risk management of food-borne parasites. Microbiological Risk Assessment Series 2014;23: 302. Available: http://www.fao.org/3/a-i3649e.pdf.
- 2. WHO. WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007–2015. 2015; 255.
- 3. Esch KJ, Petersen CA. Transmission and epidemiology of zoonotic protozoal diseases of companion animals. Clin Microbiol Rev. 2013;26(1): 58–85. pmid:23297259
- 4. Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, et al. World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLoS Med. 2015;12(12): e1001923. pmid:26633896
- 5. Ross RD, Stec LA, Werner JC, Blumenkranz MS, Glazer L, Williams GA. Presumed acquired ocular toxoplasmosis in deer hunters. Retina. 2001;21(3): 226–229. pmid:11421011
- 6. Weese JS, Peregrine AS, Armstrong J. Occupational health and safety in small animal veterinary practice: Part II—Parasitic zoonotic diseases. Can Vet J. 2002;43(10): 799–802. pmid:12395769
- 7. Deutz A, Fuchs K, Schuller W, Nowotny N, Auer H, Aspöck H, et al. [Seroepidemiological studies of zoonotic infections in hunters in southeastern Austria—prevalences, risk factors, and preventive methods]. Berl Munch Tierarztl Wochenschr. 2003;116(7–8): 306–311. pmid:12894685
- 8. Coklin T, Farber J, Parrington L, Dixon B. Prevalence and molecular characterization of Giardia duodenalis and Cryptosporidium spp. in dairy cattle in Ontario, Canada. Vet Parasitol. 2007;150(4): 297–305. pmid:17964724
- 9. Kinross P, Beser J, Troell K, Axén C, Björkman C, Lebbad M, et al. Cryptosporidium parvum infections in a cohort of veterinary students in Sweden. Epidemiol Infect. 2015;143(13): 2748–2756. pmid:25633822
- 10. Moks E, Jogisalu I, Saarma U, Talvik H, Jarvis T, Valdmann H. Helminthologic survey of the wolf (Canis lupus) in Estonia, with an emphasis on Echinococcus granulosus. J Wildl Dis. 2006:42: 359–365. pmid:16870858
- 11. Lassen B, Viltrop A, Raaperi K, Järvis T. Eimeria and Cryptosporidium in Estonian dairy farms in regard to age, species, and diarrhoea. Vet Parasitol. 2009;166(3–4): 212–219. pmid:19747778
- 12. Lassen B, Jokelainen P, Tagel M, Klaassen E, Neare K, Orro T, Viltrop A. Prevalence of antibodies against Toxoplasma gondii in Estonian cattle. In: SVEPM 2014—the Annual Conference of the Society for Veterinary Epidemiology and Preventive Medicine. 2014.
- 13. Laurimaa L, Davison J, Süld K, Plumer L, Oja R, Moks E, et al. First report of highly pathogenic Echinococcus granulosus genotype G1 in dogs in a European urban environment. Parasit Vectors. 2015:8(1): 182. pmid:25884757
- 14. Marcinkutė A, Šarkūnas M, Moks E, Saarma U, Jokelainen P, Bagrade G, et al. Echinococcus infections in the Baltic region. Vet Parasitol. 2015;213(3–4): 121–131. pmid:26324242
- 15. Must K, Lassen B, Jokelainen P.Seroprevalence of and Risk Factors for Toxoplasma gondii Infection in Cats in Estonia. Vector Borne Zoonotic Dis. 2015;15(10): 597–601. pmid:26394196
- 16. Jokelainen P, Velström K, Lassen B. Seroprevalence of Toxoplasma gondii in free-ranging wild boars hunted for human consumption in Estonia. Acta Vet. Scand. 2015;57: 42. pmid:26239110
- 17. Kärssin A, Velström K, Gómez Morales MA, Saar T, Jokelainen P, Lassen B. Cross-Sectional Study of Anti-Trichinella Antibody Prevalence in Domestic Pigs and Hunted Wild Boars in Estonia. Vector Borne Zoonotic Dis. 2016. [epub ahead of print] pmid:27315523
- 18. Jõgiste A, Varjas J, Märtin J, Aro T, Kutsar K. Communicable Disease Statistics in Estonia Part 9, Health Protection Inspectorate. Tallinn. 2000; 96. Available: http://www.terviseamet.ee/fileadmin/dok/Kasulikku/Stat_9_KOOND.pdf.
- 19. Statistics Estonia. PH193: INCIDENCE OF SELECTED REGISTERED INFECTIOUS DISEASES BY SEX. 2015. Available: http://pub.stat.ee/px-web.2001/Dialog/varval.asp?ma=PH193&lang=1.
- 20. Health Board. 2015. Nakkushaigused Eestis 1999–2005. Available: http://www.terviseamet.ee/nakkushaigused/nakkushaigustesse-haigestumine.html.
- 21. Health Board. 2015. Nakkushaigused Eestis 2006–2010. Available: http://www.terviseamet.ee/nakkushaigused/nakkushaigustesse-haigestumine.html.
- 22. Health Board. 2015. Nakkushaigused Eestis 2011–2015. Available: http://www.terviseamet.ee/nakkushaigused/nakkushaigustesse-haigestumine.html.
- 23. European Food Safety Authority. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA Journal. 2015;13.
- 24. Health Board. 2015. Available: http://www.terviseamet.ee/fileadmin/dok/Nakkushaigused/nakkused/Taenia_solium_teniaas_.pdf
- 25. Pehk R (1994) Toksoplasmoosiuuringud Tartus. Eesti Arst 1: 20–21
- 26. Birgisdóttir A, Asbjörnsdottir H, Cook E, Gislason D, Jansson C, Olafsson I, et al. Seroprevalence of Toxoplasma gondii in Sweden, Estonia and Iceland. Scand J Infect Dis. 2006;38(8): 625–631. pmid:16857606
- 27. Statistics Estonia. PO021: POPULATION BY SEX AND AGE GROUP, 1 JANUARY. 2015. Available: http://pub.stat.ee/px-web.2001/Dialog/varval.asp?ma=PO021&lang=1.
- 28. Estonian Veterinary Board, Register of licenced veterinarians. 2016. Available: http://www.vet.agri.ee/?op=body&id=928
- 29. Estonian Ministry of Environment, Hunting Department. 2016. Available: http://www.envir.ee/et/jahindus.
- 30. Sergeant ESG. Epitools epidemiological calculators. AusVet Animal Health Services and Austrailian Biosecurity Cooperative Research Centre for Emerging Infectious Diseases. Available: http://epitools.ausvet.com.au.
- 31. Dean AG, Sullivan KM, Soe MM. OpenEpi: Open Source Epidemiologic Statistics for Public Health. 2015. Available: www.OpenEpi.com.
- 32. Havelaar AH, Haagsma JA, Mangen MJ, Kemmeren JM, Verhoef LP, Vijgen SM, et al. Disease burden of foodborne pathogens in the netherlands, 2009. Int. J. Food Microbiol. 2012;156(3): 231–238. pmid:22541392
- 33. Torgerson PR. One world health: socioeconomic burden and parasitic disease control priorities. Vet Parasitol. 2013;195(3–4): 223–232. pmid:23628712
- 34. Pinelli E, Herremans T, Harms MG, Hoek D, Kortbeek LM. Toxocara and Ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands: trends from 1998 to 2009. Eur J Clin Microbiol Infect Dis. 2011;30(7): 873–879. pmid:21365288
- 35. Malafiej E, Spiewak E. Serological investigation of children infected with Ascaris lumbricoides. Wiad Paraszytol. 2001;47: 585–590. pmid:16886394
- 36. Pinelli E, Herremans T, Harms MG, Hoek D, Kortbeek LM. Toxocara and Ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands: trends from 1998 to 2009. Eur J Clin Microbiol Infect Dis. 2011;30(7): 873–879. pmid:21365288
- 37. Poeppl W, Herkner H, Tobudic S, Faas A, Mooseder G, Burgmann H, et al. Exposure to Echinococcus multilocularis, Toxocara canis, and Toxocara cati in Austria: a nationwide cross-sectional seroprevalence study. Vector Borne Zoonotic Dis. 2013;13(11): 798–803. pmid:24107202
- 38. Fotiou V, Malissiova E, Minas A, Petinaki E, Hadjichristodoulou C. Seroprevalence of IgG antibodies against Echinococcus granulosus in the population of the region of Thessaly, Central Greece. PLoS One. 2012;7(5): e37112. pmid:22615913
- 39. Żukiewicz-Sobczak W, Zwoliński J, Chmielewska-Badora J, Galińska EM, Cholewa G, Krasowska E, et al. Prevalence of antibodies against selected zoonotic agents in forestry workers from eastern and southern Poland. Ann Agric Environ Med. 2014;21(4): 767–770. pmid:25528917
- 40. Gutiérrez MP, Ramírez I, Zarzosa Mdel P, Fernández JM, Dueñas AI, Mantecón MA, et al. Seroprevalence of infection due to Echinococcus granulosus in the population of Castilla and León (Spain). Enferm Infecc Microbiol Clin. 2003;21(10): 563–567. pmid:14642255
- 41. Kiliç S, Al FD, Celebi B, Babür C. The investigation of the seroprevalence of cystic echinococcosis in veterinary surgeons. Turkiye Parazitol Derg. 2007;31(2): 109–111. pmid:17594649
- 42. Zammarchi L, Strohmeyer M, Bartalesi F, Bruno E, Muñoz J, Buonfrate D, et al. Epidemiology and management of cysticercosis and Taenia solium taeniasis in Europe, systematic review 1990–2011. PloS One. 2013;8(7): e69537. pmid:23922733
- 43. Devleesschauwer B, Allepuz A, Dermauw V, Johansen MV, Laranjo-González M, Smit GS, et al. Taenia solium in Europe: Still endemic? Acta Trop. 2015 Aug 12. pii: S0001-706X(15)30083-8. pmid:26276698
- 44. European Food Safety Authority (EFSA). Biological hazards reports. National zoonoses country reports. Available at: https://www.efsa.europa.eu/sites/default/files/assets/zoocountryreport11ee.pdf.
- 45. Ljungström I, van Knapen F. An epidemiological and serological study of toxocara infection in Sweden. Scand J Infect Dis 1989;21(1): 87–93. pmid:2727630
- 46. Stensvold CR, Skov J, Møller LN, Jensen PM, Kapel CM, Petersen E, et al. Seroprevalence of human toxocariasis in Denmark. Clin Vaccine Immunol. 2009;16(9): 1372–1373. pmid:19641098
- 47. Havasiová K, Dubinský P, Stefancíková A. A seroepidemiological study of human Toxocara infection in the Slovak Republic. J Helminthol. 1993;67: 291–296. pmid:8132974
- 48. Nicoletti A, Sofia V, Mantella A, Vitale G, Contrafatto D, Sorbello V, et al. Epilepsy and toxocariasis: a case-control study in Italy. Epilepsia 2008;49: 594–599. pmid:18031545
- 49. Kroten A, Toczylowski K, Kiziewicz B, Oldak E, Sulik A. Environmental contamination with Toxocara eggs and seroprevalence of toxocariasis in children of northeastern Poland. Parasitol Res. 2016;115(1): 205–209. pmid:26385468
- 50. Valdmann H, Moks E, Talvik H. Helminth fauna of Eurasian lynx (Lynx lynx) in Estonia. J Wildl Dis. 2004;40(2): 356–360. pmid:15362842
- 51. Talvik H, Moks E, Mägi E, Järvis T, Miller I. Distribution of Toxocara infection in the environment and in definitive and paratenic hosts in Estonia. Acta Vet Hung. 2006;54(3): 399–406. pmid:17020143
- 52. Lassen B, Jokelainen P. Survey of the presence of Toxocara spp. eggs in dog feces in Tartu, Estonia. Vector Borne Zoonotic Dis. 2016;16(3): 212–214. pmid:26854385
- 53. Pappas G, Roussos N, Falagas ME. Toxoplasmosis snapshots: Global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol 2009;39: 1385–1394. pmid:19433092
- 54. Villena I, Ancelle T, Delmas C, Garcia P, Brezin AP, Thulliez P, et al. Congenital Toxoplasmosis in France in 2007: First results from a national surveillance system. Euro Surveill. 2010;15: pii = 19600. pmid:20587361
- 55. Jokelainen P, Tagel M, Lassen B, Viltrop A. Toxoplasma gondii seropositive farm animals—a failure in prevention. In: Annual Meeting of the Society for Veterinary Epidemioplogy and Preventive Medicine–SVEPM 2016. 2016.
- 56. Møller LN, Koch A, Petersen E, Hjuler T, Kapel CM, Andersen A, et al. Trichinella infection in a hunting community in East Greenland. Epidemiol Infect. 2010;138(9): 1252–1256. pmid:20144253
- 57. Deckers N, Dorny P. Immunodiagnosis of Taenia solium taeniosis/cysticercosis. Trends Parasitol. 2010;26(3): 137–144. pmid:20083438
- 58. Tappe D, Grüner B, Kern P, Frosch M. Evaluation of a commercial Echinococcus Western blot assay for serological follow-up of patients with alveolar echinococcosis. Clin Vaccine Immunol. 2008;15: 1633–1637. pmid:18799646