Quantitative risk assessment for human Taenia saginata infection from consumption of Australian beef

Highlights

• A model for sensitivity of post-mortem inspection of cattle for C. bovis was updated.

• T. saginata infection of humans from consumption of Australian beef was modelled.

• The risk of infection was estimated to be very low in the domestic and export markets.

• Reduced post-mortem inspection resulted in negligible increase in risk.

• Incision of hearts/masseters no longer commensurate with risk.

Abstract

Humans are the primary host of the tapeworm Taenia saginata, and the tapeworm eggs are passed in human faeces. Viable eggs can be ingested by cattle and form cysts (Taenia saginata cysticercus, more commonly known as Cysticercus bovis) in their muscles. While cysts become non-viable over time, the life cycle is completed if viable cysts are ingested by humans in raw or undercooked beef. In Australia, T. saginata is not endemic in the human population and cattle are generally not grazed on pastures that have been irrigated with sewage. Nevertheless, all cattle are inspected post-mortem for lesions, including incisions of the heart and masseters, despite the lack of sensitivity of inspection when infections are light.

A Quantitative Risk Assessment (QRA) model was adapted and updated to quantify the risk of human T. saginata infection from consumption of Australian beef domestically and in key export markets. The model was used to investigate the effect of reducing current post-mortem inspection (PMI) protocols by removing the need to incise the masseters, or by removing all incisions, for low risk cattle.

The results of the QRA indicate that the risk of human T. saginata infection from consumption of Australian beef is very low—a median 0.37 (95% Credibility Interval: 0.03–10.5) and 0.27 (0.01–3.8) cases per 1 billion (10⁹) portions consumed in the domestic and top 5 export markets (USA, Japan, Korea, China and Canada), or equivalently 0.56 (0.04–15.8) and 0.97 (0.05–13.4) illness per year, respectively. Moving to reduced PMI, which only includes incisions of the heart, was estimated to result in a negligible increase in risk, equivalent to one additional infection every 12.5 and 33.3 years in the domestic and all export markets, respectively. Further reduction in PMI requirements, i.e. visual only PMI, was estimated to result in a small increase in risk to 0.7 (0.05–19.0) and 1.1 (0.06–16.5) illness per year—a median increase of about one additional case in domestic and export markets each per seven years.

The evidence present in this QRA demonstrates that alternative post-mortem inspection procedures for C. bovis achieve equivalent food safety outcomes to the current domestic standard.

Introduction

Traditional organoleptic post-mortem inspection (PMI) was developed in the late 19th and early 20th century to control important zoonotic diseases such as tuberculosis, taeniasis and trichinosis in Europe and North America when these diseases were relatively prevalent (Von Ostertag, 1892). Among these foodborne zoonoses, PMI for Taenia saginata cysticercus, more commonly referred to as Cysticercus bovis which is used throughout this text, has been a quintessential example of the effectiveness of veterinary public health which has led to substantial improvements in animal health management, whereby retention of traditional procedures is now questionable in the context of consumer risk (van der Logt, Hathaway, Vose, 1997, Dupuy, Hendrikx, Hardstaff, Lindberg, 2012, Hill, Horigan, Clarke, Dewéb, Stärk, O’Brien, Buncic, 2014). Adoption of Codex Alimentarius Commission principles and guidelines for the conduct of microbiological risk assessment and the Code of Hygienic Practice for Meat (CAC, CAC) now provide a framework for taking an evidence-based approach for the allocation of food safety resources commensurate with risk. Accordingly, risk managers increasingly utilize quantitative assessments of risk for justifying new regulation and equally for the removal of regulation when no longer applicable or effective.

This applies for Cysticercus bovis in industrialised countries where animals are generally not grazed on pastures that have been irrigated by sewage due to the risk of T. saginata infection (Rickard, Adolph, 1977, Seddon, 1967). As a result the prevalence of C. bovis in cattle tends to be low (Pearse, Traub, Davis, Cobbold, Vanderlinde, 2010, van der Logt, Hathaway, Vose, 1997) and associated infections tend to be light, i.e. involving only few cysts. For this reason it is widely acknowledged that the organoleptic inspection procedure for C. bovis lacks sensitivity (Griffiths, 1950, Murrell, 2005, Dorny, Vercammen, Brandt, Vansteenkiste, Berkvens, Geerts, 2000, Kyvsgaard, Ilsøe, Henriksen, Nansen, 1990, Pearse, Traub, Davis, Cobbold, Vanderlinde, 2010).

Based on these observations, and the low prevalence of C. bovis in New Zealand (NZ), van der Logt et al. (1997) reported the results of a quantitative risk assessment (QRA) for human infection from T. saginata from the consumption of New Zealand beef produced under the following PMI models (i) Traditional PMI using one or two incisions of the masseters (depending on market), one deep incision is made into each internal pterygoid muscle and several incisions of the heart and (ii) No PMI for cysts. Under the traditional PMI, the estimated mean number of human infections in NZ domestic and export markets were 1.10 and 0.50, respectively. Undertaking no PMI for C. bovis resulted in a marginal increase in these estimates to 1.30 and 0.61, respectively. This model was adapted (Skjerve, 1999) to the Norwegian situation to investigate the effect on human illness in Norway from importing beef from T. saginata endemic areas.

Similar to NZ, the prevalence of C. bovis in Australian cattle is estimated to be very low. The purpose of this project was to adapt the NZ QRA for C. bovis in beef to the Australian context, incorporating updates to the scientific evidence. In particular, the aim was to estimate the number of infections per year and the mean probability of human T. saginata infection from the consumption of Australian beef meat, in the domestic and key export markets in 2015. The scope of this QRA was to model C. bovis in low-risk Australian beef cattle, i.e. those reared on non-sewage irrigated pasture, slaughtered in accredited Australian abattoirs and under routine PMI practices, from slaughter to consumption in Australia and the top 5 beef export markets, and to provide evidence for adoption of alternative post-mortem inspection procedures.