All about Toxoplasma gondii infections in pigs: 2009–2020

Highlights

• Pigs are considered as the main meat source of Toxoplasma gondii infections in humans in some countries.

• This paper reviews biology of T. gondii in pigs in the last decade (2009–2019).

• Information on the spread of Chinese 1, ToxoDB genotype #9 in pigs in China is reviewed.

• Safety of ready to eat pork products with respect to T. gondii infection is discussed.

Abstract

Toxoplasma gondii infections are common in humans and animals worldwide. Toxoplasma gondii infection in pigs continues to be of public health concern. Pigs are important for the economy of many countries, particularly, USA, China, and European countries. Among the many food animals, pigs are considered the most important for T. gondii transmission in USA and China because viable parasites have rarely been isolated from beef or indoor raised chickens. Besides public health issues, T. gondii causes outbreaks of clinical toxoplasmosis in pigs in China, associated with a unique genotype of T. gondii (ToxoDB genotype #9 or Chinese 1), rarely found in other countries. The safety of ready to eat pork products with respect to T. gondii infection is a matter of recent debate. Here, we review in detail seroprevalence, prevalence of viable and nonviable T. gondii, epidemiology, risk assessment, diagnosis, and curing of pork products containing T. gondii for the past decade. This review will be of interest to biologists, parasitologists, veterinarians, and public health workers.

Introduction

The protozoan Toxoplasma gondii infects virtually all warm-blooded animals, including humans, livestock, and marine mammals (Dubey, 2010). Approximately one-third of humanity is infected with T. gondii worldwide although this varies markedly between populations (Dubey, 2010; Robert-Gangneux and Dardé, 2012). Most infections appear to be asymptomatic in immunocompetent persons; however, the parasite can cause serious disease in humans, especially neonates, and immunocompromised people, who can die of toxoplasmosis (Peyron et al., 2016). In many animal host species, the infection is also typically subclinical; however, toxoplasmosis can be fatal in many hosts (Dubey, 2010).

The ingestion of food or water contaminated with oocysts excreted by infected cats or ingesting uncooked or undercooked meat containing tissue cysts of T. gondii are the 2 major modes of transmission of T. gondii. The proportion of the human population that acquires infection by ingestion of oocysts in the environment or by eating contaminated meat is not generally known and varies with cultural habits and the environment (Boyer et al., 2011; Hill et al., 2011).

Serological surveys have indicated that up to 30% of domestic pigs have been exposed to T. gondii worldwide (Limon et al., 2017; Rostami et al., 2017; Foroutan et al., 2019) and viable T. gondii has been isolated from pork tissues obtained at slaughter (Dubey, 2010). Recently, there has been numerous articles on T. gondii infection in pigs from China, especially on association of outbreaks of clinical toxoplasmosis in pigs with a unique genotype of T. gondii (ToxoDB genotype #9) (reviewed in Dong et al., 2018; Zhang et al., 2019).

The European Food Safety Authority (EFSA) recognized T. gondii as one of the public health hazards in swine to be assessed during meat inspection (see van Asseldonk et al., 2017). A research program was initiated in The Netherlands, to study cost effectiveness of the control programs for reducing T. gondii infection in pigs (van Asseldonk et al., 2017). In the past decade, demonstration of T. gondii DNA in processed pork or in cured pork products (Bayarri et al., 2010; Herrero et al., 2017; Costa et al., 2018) has raised questions of the safety of these products with respect to T. gondii transmission. There are conflicting reports concerning the survival of T. gondii in cured pork products.

Here, we review prevalence of anti-T. gondii antibodies, viable T. gondii, and T. gondii DNA in porcine tissues, epidemiology, risk factors, clinical disease, safety of processed and cured pork products for the past decade.