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Toxoplasma Gondii Seroprevalence in Breeding Pigs in Estonia Azzurra Santoro1†, Maarja Tagel2*† , Kärt Must2, Miia Laine2, Brian Lassen2,3 and Pikka Jokelainen2,4,5

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Toxoplasma Gondii Seroprevalence in Breeding Pigs in Estonia Azzurra Santoro1†, Maarja Tagel2*† , Kärt Must2, Miia Laine2, Brian Lassen2,3 and Pikka Jokelainen2,4,5 Santoro et al. Acta Vet Scand (2017) 59:82 https://doi.org/10.1186/s13028-017-0349-1 Acta Veterinaria Scandinavica RESEARCH Open Access Toxoplasma gondii seroprevalence in breeding pigs in Estonia Azzurra Santoro1†, Maarja Tagel2*† , Kärt Must2, Miia Laine2, Brian Lassen2,3 and Pikka Jokelainen2,4,5 Abstract Background: Toxoplasma gondii is a widespread occurring parasite infecting warm-blooded animals, including pigs and humans. The aims of this study were to estimate the prevalence of anti-T. gondii antibodies and to evaluate risk factors for T. gondii seropositivity in breeding pigs raised in Estonia. Sera from 382 pigs were tested with a commercial direct agglutination test, using a cut-of titer of 40 for seropositivity, for the presence of anti-T. gondii immunoglobulin G antibodies. Results: Twenty-two (5.8%) of the 382 pigs tested seropositive for T. gondii, and 6 of the 14 herds had at least one seropositive pig. The proportion of seropositive pigs within the herds ranged between 0 and 43%. Gender appeared as a signifcant factor, with sows having 5.6 times higher odds to be seropositive to T. gondii than boars. Seropreva- lence did not increase with age. Conclusions: Anti-T. gondii antibodies were present in a substantial proportion of breeding pig herds in Estonia. On the other hand, the presence of herds without seropositive pigs illustrates that porcine T. gondii infections can be avoided even in a country where the parasite is endemic and common in several other host species. Keywords: Breeding herd, Epidemiology, Porcine, Serology, Sus scrofa domesticus, Swine, Toxoplasmosis, Zoonosis Background parasites have been isolated from unprocessed tissues Toxoplasma gondii is a protozoan parasite with world- of infected pigs as well as from commercial cuts such as wide distribution. Recently, the Food and Agriculture ham, bacon, and pork tenderloin [7, 8]. Possible sources Organization (FAO) and the World Health Organization of naturally-acquired porcine T. gondii infections have (WHO) ranked it 4th among foodborne parasites causing been investigated in studies evaluating diferent risk fac- the greatest global concern [1]. tors for porcine T. gondii infection [2, 4]. Some investi- All warm-blooded animals, including humans and pigs, gated risk factors, such as the age of the pigs and herd can host T. gondii. Both humans and pigs, being omni- size, do not provide us with useful clues regarding the vores, can acquire the infection via ingestion of tissues sources of infection, whereas others do. For example, the of other hosts that carry the parasite, via ingestion of access of seropositive juvenile cats to areas where sows oocysts from a contaminated environment, or congeni- were housed [9], direct access of cats to pig feed [10], and tally [2]. Infections with T. gondii can be subclinical, but a high density of cats at the farm [11] have been shown toxoplasmosis can have severe consequences for both to be positively associated with T. gondii seropositivity human and porcine health [3–5]. in pigs, suggesting oocyst contamination of pig feed and Pork is considered a major source of human T. gondii the farm environment as possible sources of the infec- infections in Europe and the USA [2, 6]. Viable T. gondii tion. Inadequate rodent control has also been associated with T. gondii seropositivity in pigs, suggesting infected rodents as a possible source of T. gondii infection for pigs *Correspondence: [email protected] [12]. †Azzurra Santoro and Maarja Tagel contributed equally to this work 2 Institute of Veterinary Medicine and Animal Sciences, Estonian Toxoplasma gondii infection has been reported University of Life Sciences, Kreutzwaldi 62, 51014 Tartu, Estonia in humans and pigs worldwide [2, 4]. Te European Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Santoro et al. Acta Vet Scand (2017) 59:82 Page 2 of 8 Food Safety Authority (EFSA) has listed toxoplasmosis random sampling had been used at the animal-level. among the diseases to be reported by European Union Te number of pigs that had been sampled per herd was (EU) member states according to their epidemiological 5–52. Te blood samples had been collected in 2012 by situation and emphasized the lack of representative data veterinarians of the Estonian Veterinary and Food Board. for T. gondii in humans, animals, and food [13]. Moreo- Te samples had been collected on the farms, from the ver, EFSA has included T. gondii among the most relevant jugular vein of live pigs, into vacuum tubes without rea- biological hazards in the context of meat inspection of gents. Te sera had been separated by centrifugation and swine and has pointed out that the current meat inspec- were stored at − 20 °C until analysis. tion is unable to detect the parasite [14]. Te sample size of 382 domestic pigs was evaluated to In Estonia, a recent nationwide study estimated that T. be sufcient for estimating the animal-level seropreva- gondii seroprevalence was 55.8% in the human popula- lence using the Epi Tools software calculator [25], with tion in general, and 74.4% in a separate group of animal an expected seroprevalence range of 3.2–4.2% [26, 27], caretakers [15]. Further epidemiological data from other confdence level of 95%, and population size of 15,337 host species, including domestic cats [16], cattle [17], and [24]. Ignoring clustering, the minimum required sam- wild boars [18], indicate that T. gondii is endemic also in ple size would have been 48–62 samples. Clustering these populations, and present also in the environment. was expected, thus we did not settle for the minimum Based on a EU report from 2013, none of 20 pigs tested required sample size and included all the 382 samples from Estonia were T. gondii seropositive [19]. While the that were available. consumption of pork has increased from 26.8 kg per per- son in 2002 to 44.2 kg per person in 2016 [20], there have Background information been no studies with larger sample size on prevalence of Background information for each pig was extracted from subclinical T. gondii infection in domestic pigs in Estonia. the registers of the Estonian Livestock Performance Moreover, there are no reports of clinical porcine toxo- Recording Ltd and included gender, breed, and age in plasmosis from Estonia. days and in years. Gender was unknown for 58 pigs, Te aims of our cross-sectional seroepidemiologi- breed for 87 pigs, and age for 71 pigs. For each farm, we cal study were to estimate T. gondii seroprevalence and had information about herd size and farm location. to evaluate potential risk factors for T. gondii seroposi- Te sample consisted of breeding sows (66%) and tivity in breeding pigs in Estonia. More specifcally, we boars (34%) (Table 1). Pigs that were crossbred Esto- estimated the animal-level prevalence of anti-T. gondii nian Landrace breed and Estonian Large White breed immunoglobulin G (IgG) antibodies and evaluated both were most common (36%), followed by pure Estonian animal-level and farm-level risk factors for animal-level Landrace breed (33%) and pure Estonian Large White T. gondii seropositivity. breed (18%) (Table 1). Te age of the pigs ranged from 178 to 2742 days (mean 726 days, median 651 days); that Methods is, from 6 months to 7 years (mean 1.99 years, median Study population and study design 1.78 years). Te herd size range was 58–11,295 (mean Te samples investigated were originally collected for 3786, median 2366) pigs. Seven of the farms were located national surveillance of other infectious diseases. Te in the northern part of the country and seven of the surplus of them were used in two other studies [21, 22] in farms were located in the southern part of the country addition to our study. Serology was performed blinded, (Fig. 1; divided as in [18]). and the data were coded and treated confdentially. At the end of 2011, there were 365,700 pigs in Estonia Serology [23]. Tis included 30 breeding herds with 15,337 ani- Te serum samples were tested for the presence of spe- mals, including boars used for insemination [24]. cifc IgG antibodies against T. gondii using a commercial In this cross-sectional seroepidemiological study, we direct agglutination test (Toxo-Screen DA, bioMérieux, analyzed blood samples from breeding pigs in Estonia for Marcy-l’Étoile, France), according to the manufacturer’s evidence of naturally acquired T. gondii infections. Te instructions. In this method, possible immunoglobulin M sample was a convenience sample. antibodies are denatured by 2-mercaptoethanol. Te dilution of the samples was 1:40 and pigs testing Samples positive were defned as seropositive; that is, the cut-of Te samples available for our study were sera from 382 for seropositivity was titer of 40 [18]. Only samples yield- domestic pigs from 14 breeding herds located in seven ing clear positive results (an agglutination yielding a mat of the 15 counties in Estonia (Fig. 1). Information was that covered at least half of the bottom of the well) were not available for how the herds had been selected, but interpreted as positive, whereas borderline reactions Santoro et al. Acta Vet Scand (2017) 59:82 Page 3 of 8 Fig.
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