Open Access
Volume 25, 2018
Article Number 52
Number of page(s) 5
Published online 25 September 2018

© M. Heddergott et al., published by EDP Sciences, 2018

Licence Creative CommonsThis 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 work is properly cited.


Toxoplasma gondii is an obligate intracellular protozoan and the causative agent of toxoplasmosis [9]. Unsporulated oocysts are shed into the environment by felids, which are the only definitive hosts [8]. Most mammals can become intermediate hosts after consuming raw or undercooked meat containing T. gondii tissue cysts, or food and drink with oocysts [6, 9, 21]. Meat-derived products from domestic animals and game species may represent a potential source of human infection with T. gondii and the European Food Safety Authority (EFSA) recommends the monitoring of toxoplasmosis in humans, animals and foodstuffs [11].

The roe deer (Capreolus capreolus) is the most important game species in Germany [32]. According to the German Hunting Federation (DJV), around 1.2 million animals have been harvested annually countrywide in recent years ( Despite the popularity of venison and the associated processed meats, there is currently no surveillance of T. gondii infection in German roe deer populations and little knowledge about the prevalence of the parasite in wild ungulates in Germany generally [17, 23, 29].

Here, we aim to assess the seroprevalence of T. gondii in a free-living German population of roe deer by sampling carcases that were intended for human consumption.

Material and methods


Roe deer are a legal game species in Germany that licensed hunters can harvest outside the closed season. No animals were killed in order to provide samples for this study. All animals were legally shot and the carcases made available to the authors.

Sample collection

The study was performed in the west of the German federal state of Thuringia. The total size of the study area was roughly 1800 km2 comprising the Eichsfeld, the western part of the Unstrut-Hainich and the northern part of the Wartburg administrative districts. Between 2013 and 2015, local hunters collected blood from the heart of 295 legally hunted roe deer. Animals were sampled in hunting areas across the whole study area. After centrifuging samples for 10 min at 1000g using an EBA 200 (Hettich, Tuttlingen, Germany), the sera were stored at −20 °C until analysis. The sex, age and year of sample collection were recorded for each animal. Based on the dentition of the lower jaw, animals were classified as juveniles (≤1 year), yearlings (1–2 years), or adults (≥2 years) [19, 32].

Determination of antibodies to T. gondii

A commercial kit (Toxo-Screen DA®, bioMérieux, Lyon, France) was used to perform a modified agglutination test (MAT) to analyse sera for the presence of T. gondii immunoglobulin G (IgG) antibodies. Positive and negative controls employed formalin-fixed tachyzoites as antigens. Serum samples were tested at dilutions of 1:20, 1:400, 1:1600 and 1:3200. The sensitivity and specificity of the test were maximized by using a cut-off titre of 1:20 [10]. Of all the available serological tests, the MAT is considered to be the most reliable in terms of detecting antibodies to T. gondii, especially in latently infected animals [9].

Statistical analysis

We performed a χ2-test in SPSS v.22 (SPSS Inc., Chicago, Illinois, USA) to assess the effect of sex, age class and collection year on T. gondii seroprevalence. Odds ratios (ORs) and their 95% confidence intervals (95% Cls) were calculated to assess the strength of the association between the presence of antibodies and the explanatory variables.


Toxoplasma gondii antibodies were detected in 86 of the 295 analysed roe deer (29.15%, 95% CI: 24.10–34.75). Positive results were recorded at titres between 1:20 (34.88%), 1:400 (51.16%), 1:1600 (11.63%), and 1:3200 (2.33%). The difference in seroprevalence between males and females was not statistically significant (Table 1; p = 0.328). Also, the difference in seroprevalence between collection years was not significant (Table 1; p = 0.279). In contrast, there was a significant difference in seroprevalence between the different age classes (p < 0.001), with antibodies to T. gondii more frequently detected in adults (Table 1).

Table 1.

Seroprevalence of Toxoplasma gondii in roe deer by gender, age, and collection year.


This is the first study investigating the seroprevalence of T. gondii antibodies in German roe deer. Values reported from other European roe deer populations ranged from 13% to 63% (Table 2). These previous studies used at least six different diagnostic tests (Table 2). In addition to our MAT test, the direct agglutination test (DAT) and the enzyme-linked immunosorbent assay (ELISA) have also been used frequently in this context and it has been shown that the three tests produced congruent and comparable results [13, 14, 24, 34]. Seroprevalences reported using one of these three tests ranged from 13% to 52% (Table 2). Of these, studies performed in Spain and Poland often reported substantially lower prevalence values than the 29.15% reported here, while studies from Belgium and France reported substantially higher figures. Other studies presented estimates that were in line with the estimate from the present study (Table 2).

Table 2.

Seroprevalence of Toxoplasma gondii in roe deer from Europe.

There are two previous studies that investigated the T. gondii seroprevalence in wildlife from our study region. The values of 38.3% reported for raccoons (Procyon lotor) [16] and of 24.5% reported for the European mouflon (Ovis orientalis musimon) [17] were relatively high compared to values from other European studies in these species. These authors took this as evidence of high environmental contamination with oocysts as, in addition to the presence of feral, stray, and pet cats (Felis sylvestris domesticus), the study region was located within the core distribution area of the wildcat in central Germany [16, 17]. Beral et al. [4] found a positive link between higher T. gondii antibody levels in wild boar (Sus scrofa) and the occurrence of wildcats in France. Our results do not contradict this conclusion, as the T. gondii seroprevalence in the roe deer population in the area is comparable to the values observed in the other two species. While the roe deer value obtained here is not particularly high compared to other European results (Table 2), the wildcat also occurs in the study areas in France and Belgium where a high seroprevalence was observed in roe deer. Further research on the environmental factors associated with high T. gondii seroprevalence in European wildlife is clearly needed.

Our results suggest that older roe deer had a higher seroprevalence than younger animals. Other studies on roe deer came to a similar conclusion [25, 33]. T. gondii antibodies are frequently more prevalent in older animals, since the cumulative likelihood of exposure to T. gondii increases with age and the antibodies persist for a lifetime [1, 20]. We did not identify a significant difference in seroprevalence depending on sex and year of sample collection. For at least some part of the year, both sexes have overlapping home ranges [32] and a substantial difference in exposure risks between the two sexes seems unlikely. Seroprevalence did not significantly differ between years, implying that the environmental contamination with infective oocysts remained constant throughout the study, corroborating findings from the mouflon obtained for the same region and study period [17]. It has indeed been suggested that humidity and moderate temperatures promote the survival and sporulation of the oocysts [1, 9, 13, 30].

The high seroprevalence of T. gondii antibodies in a Central German population of roe deer highlights a potential source of human infection. German hunters frequently produce home-made sausages using raw or undercooked meat. Our results suggest that this may lead to an increased risk of food-borne transmission of T. gondii. Additional studies are required to assess infection levels in venison and derived products in order to assess the risk of transmitting T. gondii to humans.


We analysed the sero-epidemiology of T. gondii infection in roe deer from a central German study population. T. gondii antibodies were present in animals of all ages. Raw or undercooked venison and its derived products may be a potential source of human infection with T. gondii.

Conflict of interest

The authors declare that they have no conflicts of interest in relation to this article.


  1. Almería S, Cabezón O, Paniagua J, Cano-Terriza D, Jiménez-Ruiz S, Arenas-Montes A, Dubey JP, García-Bocanegra I. 2018. Toxoplasma gondii in sympatric domestic and wild ungulates in the Mediterranean ecosystem. Parasitology Research, 117(3), 665–671. [CrossRef] [PubMed] [Google Scholar]
  2. Aubert D, Ajzenberg D, Richomme C, Gilot-Fromont E, Terrier ME, de Gevigney C, Game Y, Maillard D, Gibert P, Dardé ML, Villena I. 2010. Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France. Veterinary Parasitology, 171(3–4), 346–349. [CrossRef] [PubMed] [Google Scholar]
  3. Bárlová E, Sedlak K, Pavlik I, Literak I. 2007. Prevalence of Neospora caninum and Toxoplasma gondii antibodies in wild ruminants from the countryside or captivity in the Czech Republic. Journal of Parasitology, 93(5), 1216–1218. [CrossRef] [Google Scholar]
  4. Beral M, Rossi S, Aubert D, Gasqui P, Terrier ME, Klein F, Villena I, Abrial D, Gilot-Fromont E, Richomme C, Hars J, Jourdain E. 2012. Environmental factors associated with the seroprevalence of Toxoplasma gondii in wild boars (Sus scrofa), France. EcoHealth, 9(3), 303–309. [CrossRef] [PubMed] [Google Scholar]
  5. Candela MG, Serrano E, Sevila J, Leon L, Caro MR, Verheyden H. 2014. Pathogens of zoonotic and biological importance in roe deer (Capreolus capreolus): Seroprevalence in an agro-system population in France. Research in Veterinary Science, 96(2), 254–259. [CrossRef] [PubMed] [Google Scholar]
  6. Cook AJ, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenun PA, Foulon W, Semprini AE, Dunn DT. 2000. Sources of Toxoplasma infection in pregnant women: European multicenter case-control study. European Research Network on Congenital Toxoplasmosis. Births Medical Journal, 321 (7254), 142–147. [Google Scholar]
  7. De Craeyea S, Speybroeckb N, Ajzenbergd D, Dardéd ML, Collinet F, Tavernierf P, van Guchtg S, Dorny P, Diericka K. 2011. Toxoplasma gondii and Neospora caninum in wildlife: Common parasites in Belgian foxes and Cervidae? Veterinary Parasitology, 178(1–2), 64–69. [CrossRef] [PubMed] [Google Scholar]
  8. Dubey JP. 2009. History of the discovery of the life cycle of Toxoplasma gondii. International Journal of Parasitology, 39(8), 877–882. [Google Scholar]
  9. Dubey JP. 2010. Toxoplasmosis of animal and humans, 2nd edn. CRC Press: Boca Raton. p. 1–313. [Google Scholar]
  10. Dubey JP, Thulliez P, Weigel RM, Andrews CD, Lind P, Powell EC. 1995. Sensitivity and specificity of various serologic tests for detection of Toxoplasma gondii infection in naturally infected sows. American Journal of Veterinary Research, 56(8), 1030–1036. [PubMed] [Google Scholar]
  11. EFSA. 2013. Scientific Opinion on the public health hazards to be covered by inspection of meat from farmed game. EFSA, 11(6), 3264, pp 181. [CrossRef] [Google Scholar]
  12. Gaffuri A, Giacometti M, Tranquillo VM, Magnino S, Cordioli P, Lanfranchi P. 2006. Serosurvey of roe deer, chamois and domestic sheep in the central Italian Alps. Journal of Wildlife Diseases, 42(3), 685–690. [CrossRef] [PubMed] [Google Scholar]
  13. Gamarra JA, Cabezón O, Pabón M, Arnal MC, Luco DF, Dubey JP, Cortázar C, Almería S. 2008. Prevalence of antibodies against Toxoplasma gondii in roe deer from Spain. Veterinary Parasitology, 153(1–2), 152–156. [CrossRef] [PubMed] [Google Scholar]
  14. Gamble HR, Dubey JP, Lambillotte DN. 2005. Comparison of a commercial ELISA with the modified agglutination test for detection of Toxoplasma infection in the domestic pig. Veterinary Parasitology, 128(3–4), 177–181. [CrossRef] [PubMed] [Google Scholar]
  15. Gauss CBL, Dubey JP, Vidal D, Cabezón O, Ruiz-Fons F, Vicente J, Marco I, Lavin S, Cortazar C, Almería S. 2006. Prevalence of Toxoplasma gondii antibodies in red deer (Cervus elaphus) and other wild ruminants from Spain. Veterinary Parasitology, 136(3–4), 193–200. [CrossRef] [PubMed] [Google Scholar]
  16. Heddergott M, Frantz AC, Stubbe M, Stubbe A, Ansorge H, Osten-Sacken N. 2017. Seroprevalence and risk factors of Toxoplasma gondii infection in invasive raccoons (Procyon lotor) in Central Europa. Parasitology Research, 116(8), 2335–2340. [CrossRef] [PubMed] [Google Scholar]
  17. Heddergott M, Osten-Sacken N, Steinbach P, Frantz AC. 2018. Seroprevalence of Toxoplasma gondii in free-living European mouflon (Ovis orientalis musimon) hunted in central Germany. Parasite, 25, 21. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  18. Hejlíček K, Litterák I, Nezval J. 1997. Toxoplasmosis in wild mammals from the Czech Republic. Journal of Wildlife Diseases, 33(3), 480–485. [CrossRef] [PubMed] [Google Scholar]
  19. Høye TT. 2006. Age determination in roe deer: a new approach to tooth wear evaluated on known age in individuals. Acta Theriologica, 51(2), 205–214. [CrossRef] [Google Scholar]
  20. Hwang YT, Pitt JA, Quirk TW, Dubey JP. 2007. Seroprevalence of Toxoplasma gondii in mesocarnivores of the Canadian prairies. Journal of Parasitology, 93(6), 1370–1373. [CrossRef] [Google Scholar]
  21. Jones JL, Parise ME, Fiore AE. 2014. Neglected parasitic infections in the United Sates: toxoplasmosis. American Journal of Tropical Medicine and Hygiene, 90(5), 794–799. [CrossRef] [Google Scholar]
  22. Kapperud G. 1978. Survey for toxoplamosis in wild and domestic animals from Norway and Sweden. Journal of Wildlife Diseases, 14(2), 157–162. [CrossRef] [PubMed] [Google Scholar]
  23. Lutz W. 1997. Serologischer Nachweis von Antikörpern gegen Toxoplasma gondii und Leptospira bei Schwarzwild. Zeitschrift Jagdwissenschaft, 43(4), 283–287. [Google Scholar]
  24. Mainar-Jaime RC, Barbera M. 2007. Evaluation of the diagnostic accuracy of the modified agglutination test (MAT) and an indirect ELISA for the detection of serum antibodies against Toxoplasma gondii in sheep through Bayesian approaches. Veterinary Parasitology, 148(2), 122–129. [CrossRef] [PubMed] [Google Scholar]
  25. Malmsten J, Jakubek EB, Bjorkman C. 2011. Prevalence of antibodies against Toxoplasma gondii and Neospora caninum in moose (Alces alces) and roe deer (Capreolus capreolus) in Sweden. Veterinary Parasitology, 177(3–4), 275–280. [CrossRef] [PubMed] [Google Scholar]
  26. Morrondo MP, Pérez-Creo A, Prieto A, Cabanelas V, Díaz-Cac JM, Arias MS, Fernández PD, Pajares G, Remesar S, López-Sández CM, Fernández G, Díez-Baños P, Panadero R. 2016. Prevalence and distribution of infectious and parasitic agents in roe deer from Spain and their possible role as reservoirs. Italian Journal of Animal Science, 16(2), 266–274. [CrossRef] [Google Scholar]
  27. Panadero R, Painceira A, López C, Vázquez L, Paz A, Díaz P, Dacal V, Cienfuegos S, Fernández G, Lago N, Díez-Baños P, Morrondo P. 2010. Seroprevalence of Toxoplasma gondii and Neospora caninum in wild and domestic ruminants sharing pastures in Galicia (Northwest Spain). Research in Veterinary Science, 88(1), 111–115. [CrossRef] [PubMed] [Google Scholar]
  28. Sedlák K, Bartová E. 2006. Seroprevalence of antibodies to Neosprora caninum and Toxoplasma gondii in zoo animals. Veterinary Parasitology, 136(3–4), 223–231. [CrossRef] [PubMed] [Google Scholar]
  29. Tackmann K. 1997. Seroprevalence of antibodies against Toxoplasma gondii in wild boars (Sus scrofa). In: EUR 18476-COST 820 Vaccines against animal coccidioses – Annual Report 1887. Office for Official Publication of the European Communities: Luxembourg. p. 167. [Google Scholar]
  30. Smith DD, Frenkel JF. 1995. Prevalence of antibodies to Toxoplasma gondii in wild mammals of Missouri and East Central Kansas: biologic and ecologic considerations of transmission. Journal of Wildlife Diseases, 31(1), 15–21. [CrossRef] [PubMed] [Google Scholar]
  31. Sroka J, Zwoliński J, Dutkiewicz J. 2007. Seroprevalence of Toxoplasma gondii in farm and wild animals from the area of Lublin province. Bulletin of the Veterinary Institute in Pulawy, 51(4), 535–540. [Google Scholar]
  32. Stubbe C. 2008. Rehwild: Biologie-Ökologie-Bewirtschaftung. Frankh Kosmos Verlag. p. 400. [Google Scholar]
  33. Vikoren T, Tharaldsen J, Fredriksen E, Handeland E. 2004. Prevalence of Toxoplasma gondii antibodies in wild red deer, roe deer, moos, and reindeer from Norway. Veterinary Parasitology, 120(3), 159–169. [CrossRef] [PubMed] [Google Scholar]
  34. Wallander C, Frossling J, Vagsholm I, Uggla A, Lunden A. 2014. Toxoplasma gondii seroprevalence in wild boars (Sus scrofa) in Sweden and evaluation of ELISA test performance. Epidemiology & Infection, 143(9), 1913–1921. [CrossRef] [Google Scholar]
  35. Witkowski L, Czopowicz M, Nagy DA, Potarniche AV, Aoanei MA, Imomov N, Mickiewicz M, Welz M, Szaluś-Jordanow O, Kaba J. 2015. Seroprevalence of Toxoplasma gondii in wild boars, red deer and roe deer in Poland. Parasite, 22, 17. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]

Cite this article as: Heddergott M, Steinbach P, Pohl D & Frantz AC. 2018. First report on the sero-epidemiology of Toxoplasma gondii infection in German roe deer (Capreolus capreolus). Parasite 25, 52.

All Tables

Table 1.

Seroprevalence of Toxoplasma gondii in roe deer by gender, age, and collection year.

Table 2.

Seroprevalence of Toxoplasma gondii in roe deer from Europe.

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.