Does only the age of the hen matter in Salmonella enterica contamination of eggs?

Highlights

• The true prevalence of Salmonella spp. in eggs was highest at the onset of lay.

• S. Typhimurium and S. Infantis were detected in the internal egg content (yolk and albumen) at a true prevalence of 0.007 (95% CI: 0.001, 0.027).

• Environmental contamination with Salmonella did not affect the true prevalence of the same salmonellae in eggs.

• Higher egg prevalence was associated with a lower body weight, higher egg production and egg weight than the breed standard.

Abstract

Contamination of eggs with Salmonella enterica is a significant risk factor contributing to foodborne disease. Periods of peak egg contamination were identified by conducting longitudinal environmental and egg sampling in 7 layer flocks until they were 50 weeks of age. A total of 714 environmental samples and 8958 eggs were cultured using standard methods for the detection of salmonellae. Pooled egg contamination with Salmonella Typhimurium or Salmonella Infantis was detected at a true prevalence (TP) of 0.002 (95% CI = 0.001, 0.004) or 0.005 (95% CI = 0.004, 0.007), respectively. S. Typhimurium and S. Infantis were detected in individual egg components; in shell rinse at a TP of 0.014 (95% CI = 0.005, 0.038), in shell and membrane at a TP of 0.01 (95% CI = 0.003, 0.032), and in albumen and yolk content at a TP of 0.007 (95% CI = 0.001, 0.027). The concentration of salmonellae in all fractions was <1 CFU/mL. The TP of Salmonella enterica in eggs was highest at the onset of lay. Higher egg prevalence was associated with a lower body weight, higher egg production, higher egg weight and mass than the breed standard for age, and poorer feed conversion efficiency. Flock physiology appears to have an important influence on the detection of eggs contaminated with Salmonella enterica.

Introduction

In Australia, Salmonella enterica subspecies enterica serovar Typhimurium (S. Typhimurium) is the Salmonella serovar most commonly associated with outbreaks of foodborne illness and accounted for 48% of notified cases of human salmonellosis in 2011 (OzFoodNet, 2015). Eggs are frequently implicated as the source of Salmonella, with 59% of outbreaks (95% CrI = 29, 75%) and 37% of sporadic cases (95% CrI = 23, 53%) of gastroenteritis attributed to contaminated eggs in one study (Glass et al., 2016).

Outbreaks of human salmonellosis in Australia follow a strong seasonal pattern, with a peak in late summer (OzFoodNet, 2002). It is largely unknown whether the prevalence of contamination of eggs with Salmonella species also varies seasonally and whether there are factors on-farm, other than hygiene and within-flock prevalence, that may influence the likelihood of detecting Salmonella either on or in eggs. The farm or flock prevalence has been reported to be higher in the winter than in the summer (Davies and Wray, 1996), but this was not seen in a recent Australian study of free range flocks (Gole et al., 2017). No studies have quantified the effects of season, flock performance (measured against breed standard performance targets) or flock age on the prevalence of egg contamination (Coleman et al., 2005). Under experimental conditions egg contamination may be higher at the onset of lay (Okamura et al., 2007, 2010; Wigley et al., 2005) and hens challenged with S. Typhimurium during rearing have been shown to shed bacteria intermittently for 15 weeks post infection, with infected birds having increased faecal glucocorticoids at the onset of lay (Pande et al., 2016; Sharma et al., 2017). Salmonella Enteritidis, S. Pullorum and S. Gallinarum are not present in the Australian egg industry (Biosecurity Australia, 2008), providing a novel opportunity to perform studies focussed on the transmission of Salmonella serovars such as S. Typhimurium. Additionally, Australian production systems and the organisation of the industry are comparable to those of other western commercial poultry producing countries.

Studies in layer flocks indicate that flock prevalence is highly variable, even on the same sites, and that it varies by housing type, Salmonella serovar and study, with even studies performed at the same location and in the same year finding different flock prevalences (Carrique-Mas et al., 2008a,b Carrique-Mas et al., 2009; Denagamage et al., 2015; Huneau-Salaün et al., 2009; Kinde et al., 2004; Mahé et al., 2008; NSW Food Authority, 2013; Snow et al., 2007). In surveys of both retail eggs and farms, egg prevalence also varies substantially. This may be a reflection of methodology, sample size, pooling effects or egg source (Gole et al., 2013; Little et al., 2007, 2008).

Eggs may be contaminated with Salmonella externally on the shell surface, or internally in either the shell membranes or the egg content (Gantois et al., 2009). The reported prevalence of Salmonella in the internal content of eggs is much lower than on the surface, regardless of Salmonella serovar (Arnold et al., 2014a). The relative importance of internal or external contamination of eggs with Salmonella Typhimurium as a source of human infection is debated, but it is well established that internal contamination may occur even when the overall levels of contamination are low (Gantois et al., 2008; Kinde et al., 2005; Wales and Davies, 2011). Salmonella Typhimurium has been shown to colonise the reproductive organs, including the ovaries, oviducts (Gantois et al., 2008; Keller et al., 1997; Okamura et al., 2010), and the follicular tissue, as well as forming eggs (Okamura et al., 2001), and to contaminate the internal and external contents of eggs in both experimental (Hassan and Curtis III, 1997; Okamura et al., 2010; Olesiuk et al., 1972; Williams et al., 1998) and natural infections (Arnold et al., 2014a; Perales and Audicana, 1989). It can also penetrate the egg shell (Padron, 1990) and survive in the albumen for at least 24 h and multiply (Cogan et al., 2004; De Vylder et al., 2013; Guan et al., 2006; Murase et al., 2006; Okamura et al., 2001), migrate from the albumen to the yolk (Gantois et al., 2008; Guan et al., 2006) and multiply in eggs after storage (Gantois et al., 2008).

The aim of this study was to evaluate the relationship between flock performance and age, the true environmental prevalence of Salmonella spp. and the true egg prevalence of Salmonella spp. In flocks sampled longitudinally until they were 50 weeks of age.