Anatomical distribution of Toxoplasma gondii in naturally and experimentally infected lambs.

Myriam Thomas,Benoît Durand,Dominique Aubert,Isabelle Villena,Radu Blaga,Sandie Escotte-Binet,Régine Geers,Céline Robert,Annie Alliot,Guillaume Belbis

doi:10.1051/parasite/2022001

Abstract

Consumption of raw or undercooked meat containing Toxoplasma gondii tissue cysts is one of the main sources of infection for humans worldwide. Among the various species intended for human consumption, sheep appear to be a high risk for human infection. The present study focused on the detailed anatomical distribution of Toxoplasma gondii in naturally and experimentally infected lambs using fresh and frozen samples of various pieces of meat, from a public health perspective. The first objective was to rank the edible parts intended for human consumption according to the detectable parasite burden by real-time PCR targeting the 529-bp repeated element. The second objective was to evaluate the impact of freezing by comparing the detection efficiency of the quantitative PCR between fresh and frozen tissues, as imports of lamb carcasses/cuts may arrive frozen or chilled. The highest estimated parasite loads were observed in skeletal muscles, and more particularly in edible portions such as quadriceps femoris muscle, intercostal muscles, deltoid muscle and diaphragm, with a significant difference in detectable parasite burden between fresh and frozen samples (p < 0.0001) or natural and experimental infection (p < 0.0001). Thoracic and pelvic limbs (3278–1048 parasites/g muscle) were ranked at the top of the list. Toxoplasma gondii DNA was detected in all the edible parts of lamb studied. These results suggest that lamb meat represents a risk for consumers. Further investigations are needed in order to confirm these differences in larger numbers of animals and in different breeds.

Highlights

The obligate intracellular coccidian parasite, Toxoplasma gondii, is responsible for one of the most important zoonoses worldwide, toxoplasmosis, with more than one third of the global population being infected [46]
The detection of T. gondii-specific immunoglobulin G (IgG) was performed on meat juice samples by a modified agglutination test (MAT), and the presence of T. gondii DNA was determined by quantitative PCR as described below
Following oral infection with 103 sporulated oocysts of Toxoplasma gondii, specific seroconversion was detected in all three lambs, beginning with day 11 post-infection

Summary

Introduction

The obligate intracellular coccidian parasite, Toxoplasma gondii, is responsible for one of the most important zoonoses worldwide, toxoplasmosis, with more than one third of the global population being infected [46]. Experts from Food and Agriculture Organization of the United Nations (FAO) and World Health Organization (WHO) have ranked T. gondii fourth, out of 24 foodborne parasites (FBP) of global importance [6]. Consumption of raw or undercooked meat from infected warm-blooded animals is considered a major source of foodborne toxoplasmosis in humans worldwide [3, 4, 45]. In the United States, a case-control study found that raw ground beef, rare lamb or locally produced cured, dried or smoked meats are among the most important risk factors for foodborne toxoplasmosis [30]. The exact role of infected lamb in the epidemiology of toxoplasmosis in humans remains undetermined, since in Europe, lower seroprevalences have been observed in lambs than in adults [5, 20, 24, 33], with a strong correlation between indirect and direct methods of T. gondii detection [37, 38]

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