Open access peer-reviewed chapter

Prevalence, Genetic Diversity, Tissue Distribution, and Risk Factors Contributing to T. gondii Burden in Domestic Pigs

Written By

Malgorzata Jennes and Eric Cox

Submitted: 28 September 2016 Reviewed: 28 February 2017 Published: 14 June 2017

DOI: 10.5772/intechopen.68203

From the Edited Volume


Edited by Isın Akyar

Chapter metrics overview

1,624 Chapter Downloads

View Full Metrics


Toxoplasma gondii is an obligatory intracellular parasite of mammals, including humans and domestic animals. The infection with this parasite has severe clinical consequences, as it causes abortion or fetal abnormalities, encephalitis in immunocompromised humans, ocular toxoplasmosis with chorioretinitis, and it may contribute to Alzheimer disease. Therefore, an efficient control of T. gondii by prevention of the transmission to humans is strongly recommended. Pork is considered as an important source of toxoplasmosis, due to the frequent consumption of the raw or undercooked porcine meat products, a high susceptibility of pigs to the infection, and because of the numerous risk factors, contributing to the prevalence of toxoplasmosis in the pig population. The cellular and humoral immune responses, such as IgM, IgG, IFN‐gamma, and interleukin‐10 or ‐12 production, associated with the acute and chronic infection in pigs, do not prevent development of the tissue cysts, which persist lifelong within the intermediate host. Therefore, the prevalence of T. gondii in the pig population might be an useful indication of the risk associated with the consumption of the porcine meat.


  • Toxoplasma gondii
  • pigs
  • meat
  • risk factors
  • parasitic burden

1. Introduction

Toxoplasma gondii is an obligate and worldwide‐distributed intracellular parasite, causing disease in all warm‐blooded animals, which includes aquatic and terrestrial mammals and birds. The prevalence of toxoplasmosis in humans reaches, depending on the study, 33–50% of the worldwide population, regardless of the geographical location or the economic status of the inhabitants [1, 2]. The pig is, among other domestic and wild mammals, a common intermediate host for T. gondii. At the same time, it can trigger human infection via the consumption of raw, undercooked, or cured porcine meat products [3]. Therefore, pork is indicated as one of the major meat sources associated with human food borne T. gondii infection, together with Salmonella and Campylobacter [4].

Although the exact prevalence of this food pathogen, in consumption of meat, is difficult to establish, the subsequent infection rate of humans has been estimated as an average of 300 consumers per 1 infected animal [5]. In addition, nearly all tissues from a pig are used directly for the consumption or processed in other meat products without freezing or cooking, increasing in that way the chance of the transmission of the disease [1].

The naturally infected domestic pigs are considered one of the sources for toxoplasmosis in humans. The lack of an obligatory screening method for the detection of antibodies or the viable parasite in the edible tissues, respectively on farm level or in slaughterhouses, increases the risk that infected animals enter the food chain. The worldwide prevalence of 0.4–93% varies significantly between continents and countries, being determined by diverse serological techniques using different cutoff values. Overall, the results strongly depend on the detection method, the age, and the size of the sampled population. In the developed countries, a spectacular drop in the prevalence of toxoplasmosis was observed in pigs, raised indoor in a strict confinement. Interestingly, next to the management system, many other factors can contribute to the increased risk of infection in pigs in the modern farms. The rodent control is of pivotal importance, together with the proper carcass disposal. The increasing age of the animals, small size of the herd, free range or backyard pigs rather than the strict confinement housing, source of water, and feeding of goat whey to the pigs are frequently listed risk factors. Reversely, organic or biofarms increase the chance of the transmission to pigs, and indirectly, toward humans.


2. Prevalence of T. gondii in domestic pig

The global incidence of the porcine toxoplasmosis per continent and country is shown in Table 1, taking into account the origin and the age of the animals, the farm management, and the serologic assay applied [48, 49]. According to the report from European Food Safety Agency published in 2012 [50], describing the number of the foodborne zoonotic outbreaks between 2008 and 2010, the highest proportion of positive samples in PCR or serology for T. gondii across all countries was reported for sheep and goats. However, the clinical manifestation of toxoplasmosis is particularly obvious in these two species due to abortion, so it is also more likely to be confirmed, compared with other animal species, in which the more subtle signs of infection (particularly in the acute phase of the disease) may be missed. Referring to the same report, the prevalence of T. gondii‐specific antibodies in the porcine serum samples collected in all the EU‐states was 2.2% [50].

CountryOriginPrevalence (%)AssayReference [No.]
ArgentinaSows37.80MATVenturini et al. (2004) [6]
BrazilFarm25.50In‐house ELISAde Sousa et al. (2014) [7]
Slaughter19.50IFATCademartori et al. (2014) [8]
Indoor raised11.50In‐house ELISALuciano et al. (2011) [9]
Free range20.60
Farm13.40MATPiassa et al. (2010) [10]
CanadaFinisher0.74ELISA kit4Poljak et al. (2008) [11]
ChileSlaughter8.80ELISA kit4Munoz‐Zanzi et al. (2012) [12]
ChinaFinishers4.60IHATChang et al. (2013) [13]
Farm29.60In‐house ELISADu et al. (2012) [14]
Slaughter12.00IHATWu et al. (2012) [15]
Finishers24.50In‐house ELISATao et al. (2011) [16]
Mixed farm53.40ELISA kit5Yu et al. (2011) [17]
Sows14.40IHATHuang et al. (2010) [18]
Czech RepublicSlaughter36.00ELISA kit2Bartova and Sedlak (2011) [19]
FranceSlaughter2.00ELISA kit3Roqueplo et al. (2011) [20]
GermanyFinisher4.10In‐house ELISAde Buhr et al. (2008) [21]
Sows16.50IFATDamriyasa et al. (2004) [22]
IrelandFinishers4.70LATHalova et al. (2013) [23]
ItalyIndoor raised16.10IFAT, 1/16Veronesi et al. (2011) [24]
Slaughter16.30ELISA kit1Villari et al. (2009) [25]
LatviaFinishers0.40In‐house ELISADeksne and Kirjusina (2013) [26]
Free ranged6.20
MalaysiaSows0.00IFATChandrawathani et al. (2008) [27]
MexicoBackyard17.20MATAlvarado‐Esquivel et al. (2012) [28]
NepalSlaughter11.70In‐house ELISADevleesshouwer et al. (2013) [29]
PanamaIndoor raised32.10IFATCorrea et al. (2008) [30]
PeruSlaughter27.70Western blotSaavedra et al. (2004) [31]
PolandSlaughter26.40MATSroka et al. (2008) [32]
PortugalFarm9.80MATLopes et al. (2013) [33]
RomaniaBackyard30.50IFATPastiu et al. (2013) [34]
SerbiaSlaughter9.20MATKlun et al. (2011) [35]
SlovakiaSlaughter2.16ELISA kit1Turcekowa et al. (2013) [36]
SpainFinisher9.70MATGarcia‐Bocanegra et al. (2010) [37]
SwitzerlandFinishers14.00ELISA kit3Berger‐Schoch et al. (2011) [38]
Free range13.00
TaiwanSlaughter10.10LATTsai et al. (2007) [39]
The NetherlandsOrganic10.9In‐house ELISAKijlstra et al. (2008) [40]
Indoor raised0.40van der Giessen et al. (2007) [41]
Free range5.60
Organic3.00ELISA‐kit3Meerburg et al. (2006) [42]
Indoor raised0.00LATKijlstra et al. (2004) [43]
Free range4.70
USAIndoor raised2.60ELISA kit4Hill et al. (2010) [44]
Outdoor raised6.80In‐house ELISAGebreyes et al. (2008) [45]
Indoor raised1.10
Free range25.00ELISA kit4Dubey et al. (2008) [46]
Slaughter16.40Western blotSaavedra et al. (2004) [31]
VietnamFinisher23.00MATHuong et al. (2007) [47]
Free range35.70

Table 1.

Global seroprevalence of T. gondii in domestic pigs.

Adapted from Guo et al. [48].

1Institut Pourquier, Montpellier, France; 2ID Screen Toxoplasmosis Indirect, ID-Vet, Grabels, France; 3p30-ELISA; 4 SafePath Laboratories, Carlsbad, CA; 5Haitai Biological Pharmaceuticals Co., Ltd., Zhuhai, People’s Republic of China.

In general, the seroprevalence of T. gondii dropped significantly during the last decades in Europe and in the USA. Corresponding to that, a low (0.0–0.4%) to moderate (36%) prevalence was estimated on conventional pig farms in European countries [43, 48]. In the USA, a higher (25%) prevalence was detected in the free range animals than in the outdoor‐ (6.8%) or indoor‐ranged finishers (2.8%) [46, 51]. In the Netherlands, a spectacular drop was seen for the finishers (from 54 to 1.9%; Ref. [72]) and for the seropositive sows (30.9–5.6%; Ref. [41]). In the most industrialized countries, the prevalence is not higher than 5% [2]. Nevertheless, the low prevalence cannot however, prevent the high transmission rate to humans, as even as low as 1% is equal to 1 million T. gondii seropositive animals, infecting potentially 300 million humans [52]. To date, there is no obligatory screening or notification system for the detection of seropositive animals on farms or in slaughterhouses within the EU-states. These observations and the possible reasons of the decreased prevalence are discussed in detail under Section 5 (Risk factors associated with porcine toxoplasmosis).


3. Genetic diversity

Because of the high clinical relevance, the parasite has been isolated from many naturally infected animals and humans, and molecular analysis of the parasitic genome was performed using restriction fragment length polymorphism (RFLP), PCR, or random amplified polymorphism DNA [53]. The obtained data led to genetic identification of the isolated parasites; and therefore, allowed to distinguish three major multilocus genotypes of T. gondii. The genetic lines named I, II, and III correspond to the genetic analysis of the polymorphic surface antigen 2 locus (SAG2) [54] and are characterized by a different degree of virulence and pathogenicity in LD50 in mice. Type I is considered as the most virulent genotype, followed by type III and type II. The latter is the most prevalent type present in animal reservoir and human population throughout Europe. Additionally, next to the typical three lineages, some of the strains obtained from South America, Africa, and Asia show an atypical genome or a mixed genotype of the existing ones. These strains are often characterized by an increased virulence in mice [2, 55]. Concerning the genotypes of pigs’ isolates, the majority of the strains circulating within the porcine population in North America belong to the genotypes II and III or has a mixed allele composition, while in Europe, genotype II seems to be the most predominant clonal type [56, 57]. In South America, on the contrary, genotype I or mixed types are prevalent in domestic pigs [58].


4. Immune responses and tissue distribution upon acute and chronic toxoplasmosis

Upon infection with the parasite, the humoral and cellular immune responses are initiated, while clinically toxoplasmosis in pigs proceeds mainly asymptomatic. Only occasionally, pigs develop clinical signs. Following experimental inoculation of pigs with any infectious stage of T. gondii (oocysts, tissue cysts, or tachyzoites), a range of antibodies develops against the parasitic antigens. The time interval between the inoculation and the first detection of the immunoglobulins or cytokines varies depending on the virulence of the used strain, the infectious stage, and the applied dose [37, 5962].

Secondly, a significant Th1‐immune response can be observed as an increase of IFN‐γ production after inoculation of pigs with a well‐defined number of the infectious T. gondii strains [61, 6365]. This increase is positively correlated with the duration of the experiment and can be detected in the serum collected from the infected animals in the supernatant from cultured PBMCs, and also as IFN‐γ mRNA expression in PBMCs and intestinal lymphoid tissues. The IFN‐γ production associated with the induced toxoplasmosis in pigs was in this case the result of the activation of the innate and acquired immune system. These immune responses were investigated in vitro by determining the cytokine profile until 14 [61], 40 [63], or 56 dpi [66].

Next to IFN‐γ, other cytokines are involved in the immune response. The infection of pigs with the VEG‐strain oocysts induced a Th‐1 immune response shortly after the inoculation, with the production of IL‐15 and TNF‐α mRNA [61]. Subsequently, a Th‐2 response profile with IL‐10 as anti‐inflammatory cytokine was detected after the acute phase of the infection, dominated by IFN‐γ production [63].

During the acute phase of the infection, the immune responses are directed against the disseminating tachyzoites, while throughout the chronic toxoplasmosis they also target the latent cysts with bradyzoites in the variety of tissues. It is well described that the parasite can persist within the intermediate host for a life span and can be found in all internal organs and muscles [6769]. For instance, in pigs, viable T. gondii was recovered from porcine brain, heart, tongue, diaphragm, liver, and kidneys. Additionally, all edible commercial cuts of meat tested are also positive, representing thereby, a potential risk for consumers [4, 70]. It is a subject of discussion and ongoing research whether the host can clear the tissues during the chronic infection phase. In pigs, there is a scientific evidence that tissue cysts can gradually decrease in number and show a decline in viability, as tested by bioassay [66].


5. Risk factors associated with the porcine toxoplasmosis

Several factors can potentially modify the risk of T. gondii infection in pigs, such as the presence of cats on farms, rodent control, age of the animals, size and type of the herd, outdoor access, the carcass disposal, and feeding of unprocessed animal products such as goat whey to the pigs [41, 44, 49, 71].

The cat is responsible for the direct transmission of toxoplasmosis to farm animals such as pigs by entering the stables and shedding the oocysts in the animal facilities, or by contaminating the environment, and indirect spread of oocyts by animals entering the stables like dogs or birds. The free access to stables for people, without the application of strict hygienic measures (e.g., disinfecting foot bath or protective footwear and clothes for the exclusive use in the animal facilities) can also contribute to the dissemination of the oocysts within the herd or its transmission to the stables from the contaminated environment. The lack of these measures is especially important if domesticated or feral cats live in the close neighborhood of the animal facilities.

The second factor, namely the insufficient rodent control in the stables drives the persistence of the parasite on farm level in two ways: the rodents serve as a constant reservoir of the parasite for the cats, maintaining directly the infection risk within the herd; additionally, the rodents can directly be involved in the infection transmission by the predation or accidental ingestion of the mice by pigs [40, 56].

Age as a risk factor is strictly associated with a longer exposure and evidenced by an increased seroprevalence in older animals in comparison with piglets. As colostral antibodies disappear by 120 days of age, piglets and young raising pigs do not have any maternal immune protection, and are, therefore, exposed to the infection [71]. However, the humoral immunity alone is not sufficient in combating the parasite. Indeed, the antibodies facilitate the cytotoxicity by the innate immune cells toward the extracellular parasite, but the intracellular T. gondii can escape from that. The age‐dependent increase in seroprevalence in pig farms have been described in numerous studies, showing a higher incidence in adult pigs (19.5%) than in young animals (10.9%) [28], or in breeding sows than in finishers (30.9% and 1.9%, respectively, in the Netherlands [72] and 24.2% and 9.7%, respectively, in Spain [28].

The age of the animals at slaughter has also an important implication for the transmission of the disease toward human consumers and the epidemiology of human toxoplasmosis. Indeed, the younger the animals, the more chance that the meat will be consumed fresh and unprocessed, while the meat derived from older animals such as sows, will undergo processing to different pork products, which is harmful for the parasite and thus, safer for the consumer in terms of parasitic load [49].

Two major factors contributing to porcine toxoplasmosis are the size of the herd and the management type of the herd with a reverse correlation between the size and the on‐farm prevalence: small herds showed a higher rate of seropositive animals (4.1%) than medium (1.9%) or large (0.6%) herds [51]. The reason for that would be the higher exposure per animal in smaller farms due to the lower density of the pigs. Even more critical for the risk for toxoplasmosis is the management type of the farm. The recently observed decrease in seroprevalence of toxoplasmosis in the pig population in the developed countries might be due to the implementation of the modern management system in porcine herds, with a visible shift from housing of a smaller number of animals in less strictly confined establishments or outdoor, to large scale facilities with a high output and a fast turn‐over, characterized by all‐in‐all‐out or farrow‐to‐finish models [44, 48, 73]. The extensive pig production expressed by the increasing number and size of porcine herds is driven by the high consumption of porcine meat in the developed countries in Europe and in the USA. In Belgium for instance, the total yearly number of pigs comprise 6.5 million animals, housed in 5000 conventional farms, ranging between on average 700–1300 pigs, as estimated by the National Institute of the Calculations, Federal Public Service Economy, (Actualization of the Industrial Study on Pork, 2015). Consequently, nearly 12 million of animals are slaughtered each year, due to an excessive consumption rate per inhabitant (35 kg/year), in comparison with other countries.

Summarizing, in the modern large‐scale herds, the risk of T. gondii infection and thus, the prevalence of seropositive animals can be substantially reduced by the employment of a strict confinement housing with restrictive biosecurity regulations [1, 44, 45, 48].

However, in the last years, a new tendency in animal husbandry deserves the attention, namely the animal‐friendly herds, housing organic or free range animals, providing daily a permanent or a temporary outdoor access to the animals. The term ‘organic’ refers to the quality and safety of the porcine products, with constraints about the chemical compounds originating from the feed or drug treatment, while ‘free range’ stands for the life quality of the animals during the production round. Hence, organic pigs are mainly reared outdoor, receive an organic feed, are provided with an animal friendly living space, the piglets are weaned at the later age than 3–4 weeks as on the intensive farms, and undergo a restrictive use of the antibiotics. The free range pigs differ from the regular pigs by the outdoor access and straw bedding, but are fed with a standard porcine feed and may receive drug treatment, if necessary, without losing a label as in case of the organic pigs [43]. In both types of farming, pigs are continuously exposed to the parasite by contact with contaminated soil or ground water, and can easily transmit the infection further in the food chain [43, 44, 74].

As indicated above, an appropriate rodent control is of significant importance for the reduction of the risk for porcine toxoplasmosis; in addition to the latter, a proper carcass disposal seems to be equally essential, since both measures are intended to avoid the ingestion of formerly infected tissues [44, 56]. The cases of cannibalism by the accidental access to preliminary dead animals, especially when animal tissues are buried or composted are considerably common [41, 44, 49, 71]. Similarly, providing drink water of unknown quality to the pigs, possibly contaminated with the oocysts and feeding of raw animal products such as goat whey is also a potential risk, if made from unprocessed milk containing tachyzoites from a recently infected animal undergoing the dissemination phase [42, 75].

Finally, the prevalence of porcine toxoplasmosis may be influenced by the climate and geographical factors, for example, in altitude, temperature, and humidity, since they have a direct impact on the survival of T. gondii oocysts in the environment. As established previously, the oocysts remain infectious for a long period of time in a humid and cold environment, as long as they are not dried out or frozen. Hence, the prevalence of toxoplasmosis in pigs is higher in the mountains (32.1%) than in semi desert areas in Mexico (14%) [28], or in the coastal and northern regions of the USA (2.9–3.2%) than in the south continental part of the country [76].



Belgian Federal Public Service of Health, Food Chain Safety and Environment through the contract RF 13/6274 for its support


  1. 1. Tenter, A.M., Heckeroth, A.R. and Weiss, L.M. (2000). Toxoplasma gondii: From animals to humans. Int J Parasitol 30, 1217–1258.
  2. 2. Robert‐Gangneux, F. and Dardé, M.L.. (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 25 (2): 264–296.
  3. 3. Cook, A.J.C., Gilbert, R.E., Buffolano, W., Zufferey, J., Petersen, E., Jenum, P.A., Foulon, W., and Semprini, A.E. (2000). Sources of toxoplasma infection in pregnant women: European multicentre case‐control study. BMJ 321 (July): 142–147.
  4. 4. Opsteegh, M., Schares, G. and van der Giessen, J., on behalf of the consortium (2016). Relationship between seroprevalence in the main livestock species and presence of Toxoplasma gondii in meat (GP/EFSA/BIOHAZ/2013/01). An extensive literature review. Final report. In: EFSA Supporting Publication 2016, Parma, Italy: EN‐996, 294 p.
  5. 5. Fehlhaber, K., Hintersdorf, P., Kruger, G. (2002). [Study on the prevalence of Toxoplasmagondii in pigs of different management systems and in minced meat]. Fleischwirtschaft 83, 97–99.
  6. 6. Venturini, M.C., Bacigalupe, D., Venturini, L., Rambeaud, M., Basso, W., Unzaga, J.M. and Perfumo, C.J. (2004). Seroprevalence of Toxoplasma gondii in sows from slaughterhouses and in pigs from an indoor and an outdoor farm in Argentina. Vet Parasitol 124: 161–165.
  7. 7. de Sousa, R.Á., Lemos, J.F., Farias, L.A., Lopes, C.D. and dos Santos, K.R. (2014). Seroprevalence and risk factors for Toxoplasma gondii infection in pigs in southern Piauí. Braz J Vet Parasitol 23:98–100.
  8. 8. Cademartori, B.G., Santos, L.M.J.F., Oliveira, F.C., Quevedlo, P., Oliveira, P.A., Ramos, T.S., Rocha, A.S.R., Ruas, J.L. and Farias, N.A.R. (2014). Isolation and pathogenicity of Toxoplasma gondii in naturally infected (rustic farm) pigs in southern Brazil. Vet Parasitol. 203:207–211.
  9. 9. Luciano, D.M., Menezes, R.C., Ferreira, L.C., Nicolau, J.L., das Neves, L.B., Luciano, R.M., Dahroug, M.A., and Amendoeira, M.R. (2011 Oct–Dec). Occurrence of anti‐Toxoplasma gondii antibodies in cattle and pigs slaughtered, State of Rio de Janeiro. Rev Bras Parasitol. 20(4):351–353.
  10. 10. Piassa, F.R., de Araú jo, J.B., da Rosa, R.C., Mattei, R.J., da Silva, R.C., Langoni, H., and da Silva, A.V. (2010). Prevalence and risk factors for Toxoplasma gondii infection in certified and non‐certified pig breeding farms in the Toledo microregion, PR, Brazil. Rev Bras Parasitol Vet 19:152–156.
  11. 11. Poljak, Z., Dewey, C.E., Friendship, R.M., Martin, S.W., Christensen, J., Ojkic, D., Wu, J., and Chow, E. (2008). Pig and herd level prevalence of Toxoplasma gondii in Ontario finisher pigs in 2001, 2003, and 2004. Can J Vet Res. 72:303‐310. Pulawy 52:545–549.
  12. 12. Munoz‐Zanzi, C., R. Tamayo, J. Balboa, and D. Hill (2012). Detection of oocyst‐associated toxoplasmosis in swine from southern Chile. Zoonoses Public Health 59:389–392.
  13. 13. Chang, Q. C., Qiu, J.H., Wang, C.R., and Zhu, X.Q. (2013). Seroprevalence of Toxoplasma gondii infection in fattening pigs in northeast China. J Parasitol 99:544–545.
  14. 14. Du, F., Zhang, Q., Yu, Q., Hu, M., Zhou, Y., and Zhao, J. (2012). Soil contamination of Toxoplasma gondii oocysts in pig farms in central China. Vet Parasitol 187:53–56.
  15. 15. Wu, D., Lv, R., Sun, X., Shu, F., Zhou, Z., Nie, K., Duan, G., and Zou, F. (2012). Seroprevalence of Toxoplasma gondii antibodies from slaughter pigs in Chongqing, China Trop Anim Health Prod 44:685–687.
  16. 16. Tao, Q., Wang, Z., Feng, H., Fang, R., Nie, H., Hu, M., Zhou, Y. and Zhao, J. (2011). Seroprevalence and risk factors for Toxoplasma gondii infection on pig farms in central China. J Parasitol 97:262–264.
  17. 17. Yu, H.J., Zhang, Z., Liu, Z., Qu, D.F., Zhang, D.F., Zhang, H.L., Zhou, Q.J., and Du, A.F. (2011). Seroprevalence of Toxoplasma gondii infection in pigs, in Zhejiang Province, China J Parasitol 97:748–749.
  18. 18. Huang, C.Q., Lin, Y.Y., Dai, A.L., Li, X.H., Yang, X.Y., Yuan, Z.G., and Zhu, X.Q. (2010). Seroprevalence of Toxoplasma gondii infection in breeding sows in western Fujian Province, China Trop Anim Health Prod 42:115–118.
  19. 19. Bártová, E., and Sedlák, K. (2011). Seroprevalence of Toxoplasma gondii and Neospora caninum in slaughtered pigs in the Czech Republic. Parasitology 138:1369–1371.
  20. 20. Roqueplo, C., Halos, L., Cabre, O., and Davoust, B. (2011). Toxoplasma gondii in wild and domestic animals from New Caledonia. Parasite 18:345–348.
  21. 21. de Buhr, K., Ludewig, M., and Fehlhaber, K. (2008). Toxoplasma gondii—seroprevalence: Current results in German swine herds. Arch Lebensmittelhyg. 59:5–8.
  22. 22. Damriyasa, I.M., Bauer, C., Edelhofer, R., Failing, K., Lind, P., Petersen, E., Schares, G., Tenter, A.M., Volmer, R., and Zahner, H. (2004). Cross‐sectional survey in pig breeding farms in Hesse, Germany: Seroprevalence and risk factors of infections with Toxoplasma gondii, Sarcocystis spp. and Neospora caninum in sows. Vet Parasitol 126:271–286.
  23. 23. Halová, D., Mulcahy, G., Rafter, P., Turcekova, L., Grant, T., and de Waal, T. (2013). Toxoplasma gondii in Ireland: Seroprevalence and novel molecular detection method in sheep, pigs, deer and chickens. Zoonoses Public Health 60:168–173.
  24. 24. Veronesi, F., Ranucci, D., Branciari, R., Miraglia, D., Mammoli, R., and Fioretti, D.P. (2011). Seroprevalence and risk factors for Toxoplasma gondii infection on finishing swine reared in the Umbria region, central Italy. Zoonoses Public Health 58:178–184.
  25. 25. Villari, S., Vesco, G., Petersen, E., Crispo, A., and Buffolano, W. (2009). Risk factors for toxoplasmosis in pigs bred in Sicily, southern Italy. Vet Parasitol 161:18.
  26. 26. Deksne, G., and Kirjusina, M. (2013). Seroprevalence of Toxoplasma gondii in domestic pigs (Sus scrofa domestica) and wild boars (Sus scrofa) in Latvia. J Parasitol 99:44–47.
  27. 27. Chandrawathani, P., Nurulaini, R., Zanin, C.M., Premaalatha, B., Adnan, M., Jamnah, O., Khor, S.K., Khadijah, S., Lai, S.Z., Shaik, M.A.B., Seah, T.C., and Zatil, S.A. (2008). Seroprevalence of Toxoplasma gondii antibodies in pigs, goats, cattle, dogs and cats in peninsular Malaysia. Trop Biomed. 25:257–258.
  28. 28. Alvarado‐Esquivel, C., Estrada‐Malacó, n M.A., Reyes‐Hernández, S.O., Pérez‐Ramírez, J.A., Trujillo‐López, J.I., Villena, I. and Dubey, J.P. (2012). High prevalence of Toxoplasma gondii antibodies in domestic pigs in Oaxaca State, Mexico. J Parasitol 98:1248–1250.
  29. 29. Devleesschauwer, B., Pruvot, M., Joshi, D.D., De Craeye, S., Jennes, M., Ale, A., Welinski, A., Lama, S., Aryal, A., Victor, B., Duchateau, L., Speybroeck, N., Vercruysse, J., Dorny, P. (2013 Dec). Seroprevalence of zoonotic parasites in pigs slaughtered in the Kathmandu Valley of Nepal. Vector Borne Zoonotic Dis. 13(12):872–876. doi: 10.1089/vbz.2013.1313.
  30. 30. Correa, R., Cedeño, I., de Escobar, C., and Fuentes, I. (2008). Increased urban seroprevalence of Toxoplasma gondii infecting swine in Panama. Vet Parasitol. 153:9–11.
  31. 31. Saavedra, G.M., and Ortega, Y.R. (2004). Seroprevalence of Toxoplasma gondii in swine from slaughterhouses in Lima, Peru, and Georgia, U.S.A. J Parasitol 90:902–904.
  32. 32. Sroka, J., Cencek, T., Ziomko, I., Karamon, J., and Zwolinski, J. (September 2008). Preliminary assessment of ELISA, MAT, and LAT for detecting Toxoplasma gondii antibodies in pigs. Bull Vet Inst. in Pulawy, 52(4): 545–549.
  33. 33. Lopes, A.P., Dubey, J.P., Neto, F., Rodrigues, A., Martins, T., Rodrigues, M., and Cardoso, L. (2013). Seroprevalence of Toxoplasma gondii infection in cattle, sheep, goats and pigs from the north of Portugal for human consumption. Vet Parasitol. 193:266–269, 44
  34. 34. Pastiu, A.I., Gyorke, A., Blaga, R., Mircean, V., Rosenthal, B.M., and Cozma, V. (2013). In Romania, exposure to Toxoplasma gondii occurs twice as often in swine raised for familial consumption as in hunted wild boar, but occurs rarely if ever among fattening pigs raised in confinement. Parasitol Res. 112:2403–2407.
  35. 35. Klun, I., Vujanić, M., Yera, H., Nikolić, A., Ivović, V., Bobić, B., Bradonjić, S., Dupouy‐Camet, J. and Djurković‐Djaković, O. (2011). Toxoplasma gondii infection in slaughter pigs in Serbia: Seroprevalence and demonstration of parasites in blood. Vet Res 42:17–22.
  36. 36. Turcekova, L., Antolova, D., Reiterova, K., and Spisak, F. (2013). Occurrence and genetic characterization of Toxoplasma gondii in naturally infected pigs. Acta Parasitol. 58:361–366.
  37. 37. Garcia, J.L., Gennari, S.M., Navarro, I.T., Machado, R.Z., Sinhorini, I.L., Freire, R.L., Marana, E.R., Tsutsui, V., Contente, A.P., Begale, L.P. (2005). Partial protection against tissue cysts formation in pigs vaccinated with crude rhoptry proteins of Toxoplasma gondii. Vet Parasitol 129(3/4):209–217.
  38. 38. Berger‐Schoch, A.E., Bernet D., Doherr, M.G., Gottstein, B., and Frey, C.F. (2011). Toxoplasma gondii in Switzerland: A serosurvey based on meat juice analysis of slaughtered pigs, wild boar, sheep and cattle. Zoonoses Public Health 58:472–478.
  39. 39. Tsai, Y.J., Chung, W.C., Fei, A.C.Y., Kaphle, K., Peng, S. and Wu, Y.L. (2007). Seroprevalence of Toxoplasma gondii in pigs from slaughterhouses in Taiwan. J Parasitol 93:1540–1541.
  40. 40. Kijlstra, A. and Jongert, E. (October 2008). Control of the risk of human toxoplasmosis transmitted by meat. Int J Parasitol. 1359–1370.
  41. 41. van der Giessen, J., Fonville, M., Bouwknegt, M., Langelaar, M., and Vollema, A. (2007). Seroprevalence of Trichinella spiralis and Toxoplasma gondii in pigs from different housing systems in The Netherlands. Vet Parasitol 148:371–374.
  42. 42. Meerburg, B.G., van Riel, J.W., Cornelissen, J.B., Kijlstra, A., and Mul, M.F. (2006). Cats and goat whey associated with Toxoplasma gondii infection in pigs. Vector Borne Zoonotic Dis 6:266–274.
  43. 43. Kijlstra, A., Eissen, O.A., Cornelissen, J., Munniksma, K., Eijck, I., and Kortbeek, T. (2004). Toxoplasma gondii infection in animal friendly pig production systems. Invest Ophthalmol Vis Sci 45: 3165–3169.
  44. 44. Hill, D.E., Haley, C., Wagner, B., Gamble, H.R., and Dubey, J.P. (2010). Seroprevalence of and risk factors for Toxoplasma gondii in the US swine herd using sera collected during the National Animal Health Monitoring Survey (Swine 2006). Zoonoses Public Health 57:53–59.
  45. 45. Gebreyes, W.A., Bahnson, P.B., Funk, J.A., McKean, J., and Patchanee, P. (2008). Seroprevalence of Trichinella, Toxoplasma, and Salmonella in antimicrobial‐free and conventional swine production systems. Foodborne Pathog Dis. 5:199–203.
  46. 46. Dubey, J.P., Hill, D.E., Sundar, N., Velmurugan, G.V., Bandini, L.A., Kwok, O.C.H., Pierce, V., Kelly, K., Dulin, M., Thulliez, P., Iwueke, C., and Su, C. (2008). Endemic toxoplasmosis in pigs on a farm in Maryland: Isolation and genetic characterization of Toxoplasma gondii. J Parasitol 94:36–41.
  47. 47. Huong, L.T.T., and Dubey, J.P. (2007). Seroprevalence of Toxoplasma gondii in pigs from Vietnam. J Parasitol 93:951–952.
  48. 48. Guo, M., Dubey, J.P., Hill, D., Buchanan, R.L., Gamble, H., Jones, J.L., Pradhan, A.K. (2015). Prevalence and risk factors for Toxoplasma gondii infection in meat animals and meat products destined for human consumption. J Food Prot 78, 457–476.
  49. 49. Dubey, J.P. (2009 Oct 14). Toxoplasmosis in pigs – The last 20 years. Vet Parasitol 164(2‐4):89‐103. doi: 10.1016/j.vetpar.2009.05.018. Review.
  50. 50. European Food Safety Authority, European Centre for Disease Prevention and Control 2012. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2010; EFSA Journal; 10(3):2597. [442 pp.] doi:10.2903/j.efsa.2012.2597
  51. 51. Hill D.E., Chirukandoth, S., Dubey J.P., Lunney, J.K., Gamble, H.R. (2006 Oct 10). Comparison of detection methods for Toxoplasma gondii in naturally and experimentally infected swine. Vet Parasitol. 141(1‐2):9–17.
  52. 52. Jones J.L., and Dubey, J.P. (2012 Sep). Foodborne toxoplasmosis Clin Infect Dis. 55(6): 845–851. doi: 10.1093/cid/cis508. Review.
  53. 53. Sibley, L.D., LeBlanc, A.J., Pfefferkorn, E.R., Boothroyd, J.C. (1992 Dec). Generation of a restriction fragment length polymorphism linkage map for Toxoplasma gondii. Genetics. 132(4):1003–1015.
  54. 54. Howe, D.K., Sibley, L.D. (1997 Oct). Development of molecular genetics for Neospora caninum: A complementary system to Toxoplasma gondii. Methods. 13(2):123–133.
  55. 55. Innes, E.A. (2010 Feb). A brief history and overview of Toxoplasma gondii. Zoonoses Public Health. 57(1):1–7. doi: 10.1111/j.1863‐2378.2009.01276.x. Review.
  56. 56. Lehmann, T., Graham, D.H., Dahl, E., Sreekumar, C., Launer, F., Corn, J.L., Gamble, H.R., Dubey, J.P. (2003 Jul). Transmission dynamics of Toxoplasma gondii on a pig farm. Infect Genet Evol. 3(2):135–141.
  57. 57. de Sousa, S., Ajzenberg, D., Canada, N., Freire, L., da Costa, J.M., Dardé, M.L., Thulliez, P., Dubey, J.P. (2006 Jan 30). Biologic and molecular characterization of Toxoplasma gondii isolates from pigs from Portugal. Vet Parasitol. 135(2):133‐136. Epub 2005 Sep 26.
  58. 58. Belfort‐Neto, R., Nussenblatt, V., Rizzo, L., Muccioli, C., Silveira, C., Nussenblatt, R., Khan, A., Sibley, L.D., Belfort, R. Jr. (Mar 2007). High prevalence of unusual genotypes of Toxoplasma gondii infection in pork meat samples from Erechim, Southern Brazil. An Acad Bras Cienc. 79 1 Rio de Janeiro.‐37652007000100013.
  59. 59. Dubey, J.P. (1986). A review of toxoplasmosis in pigs. Vet Parasitol 19: 181–223.
  60. 60. Lind, P., Haugegaard, J., Wingstrand, A., Henriksen, S.A. (1997). The time course of the specific antibody response by various ELISAs in pigs experimentally infected with Toxoplasma gondii. Vet Parasitol 71, 1–15.
  61. 61. Dawson, H.D., Beshah, E., Nishi, S., Solano‐Aguilar, G., Morimoto, M., Zhao, A., Madden, K.B., Ledbetter, T.K., Dubey, J.P., Shea‐Donohue, T., Lunney, J.K., Urban, J.F. Jr. (2005). Localized multigene expression patterns support an evolving Th1/ Th2‐like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infect Immun 2005 Feb;73(2):1116–28.
  62. 62. Jongert, E., Melkebeek, V., De Craeye, S., Dewit, J., Verhelst, D., Cox, E. (2008a). An enhanced GRA1‐GRA7 cocktail DNA vaccine primes anti‐Toxoplasma immune responses in pigs. Vaccine 26, 1025–1031.
  63. 63. Solano Aguilar, G.I., Beshah, E., Vengroski, K.G., Zarlenga, D., Jauregui, L., Cosio, M., Douglass, L.W., Dubey, J.P., Lunney, J.K. (2001 Feb). Cytokine and lymphocyte profiles in miniature swine after oral infection with Toxoplasma gondii oocysts. Int J Parasitol. 31(2):187–195. Erratum in: Int J Parasitol 2001 Jun;31(8):852.
  64. 64. Dawson, H.D., Royaee, A.R., Nishi, S., Kuhar, D., Schnitzlein, W.M., Zuckermann, F., Urban, J. Jr., Lunney, J.K.. (2004 Jul). Identification of key immune mediators regulating T helper 1 responses in swine. Vet Immunol Immunopathol. 100(1‐2):105–111.
  65. 65. Verhelst, D., De Craeye, S., Jennes, M., Dorny, P., Goddeeris, B., Cox, E. (2015). Interferon‐gamma expression and infectivity of Toxoplasma infected tissues in experimentally infected sheep in comparison with pigs. Vet Parasitol 207 (2015) 7–16.
  66. 66. Verhelst, D., De Craeye, S., Melkebeek, V., Goddeeris, B., Cox, E., Jongert, E. (2011 Jun 30). IFN‐γ expression and infectivity of Toxoplasma infected tissues are associated with an antibody response against GRA7 in experimentally infected pigs. Vet Parasitol. 179 (1‐3):14–21.
  67. 67. Dubey, J.P., Lindsay, D.S., Speer, C.A. (1998 Apr). Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev. 11(2):267–299. Review.
  68. 68. Black, M.W., and Boothroyd, J.C. (2000). Lytic cycle of Toxoplasma gondii. Microbiology and Molecular Biology Reviews, 64, 3, pp. 607–623.
  69. 69. Montoya, J.G., Liesenfeld, O. (2004 Jun 12). Toxoplasmosis. Lancet. 363(9425):1965–1976.
  70. 70. Dubey, J.P. (1988). Long‐term persistence of Toxoplasma gondii in tissues of pigs inoculated with T. gondii oocysts and effect of freezing on viability of tissue cysts in pork. Am J Vet Res. 1988 Jun;49(6):910–913.
  71. 71. García‐Bocanegra, I., Simon‐Grifé, M., Dubey, J.P., Casal, J., Martín, G.E., Cabezó n, O., Perea, A., and Almería, S. (2010). Seroprevalence and risk factors associated with Toxolasma gondii in domestic pigs from Spain. Parasitol Int. 59:421–426.
  72. 72. van Knapen, F., Kremers, A.F., Franchimont, J.H., Narucka, U. (1995 Sep). Prevalence of antibodies to Toxoplasma gondii in cattle and swine in The Netherlands: Towards an integrated control of livestock production. Vet Q. 17(3):87–91.
  73. 73. Davies, P.R., Morrow, W.E., Deen, J., Gamble, H.R., Patton, S. (1998 Jul 17). Seroprevalence of Toxoplasma gondii and Trichinella spiralis in finishing swine raised in different production systems in North Carolina, USA. Prev Vet Med. 36(1):67–76.
  74. 74. Dubey J.P., Hill, D.E., Rozeboom, D.W., Rajendran, C., Choudhary, S., Ferreira, L.R., Kwok, O.C., Su, C. 2012 Aug 13 High prevalence and genotypes of Toxoplasma gondii isolated from organic pigs in northern USA. Vet Parasitol. 188(1‐2):14–18. doi: 10.1016/j.vetpar.2012.03.008.
  75. 75. Boughattas, S. (2015 Oct 14). Toxoplasma infection and milk consumption: Meta‐analysis of assumptions and evidences. Crit Rev Food Sci Nutr. 0.
  76. 76. Hill, D.E., and Dubey, J.P. (2013). Toxoplasma gondii prevalence in farm animals in the United States. Int J Parasitol. 43(2):107–113. doi: 10.1016/j.ijpara.2012.09.012. Review.

Written By

Malgorzata Jennes and Eric Cox

Submitted: 28 September 2016 Reviewed: 28 February 2017 Published: 14 June 2017