Microbiological contamination of shell eggs produced in conventional and free-range housing systems M.A. Parisi a , J.K. Northcutt a, * , D.P. Smith b , E.L. Steinberg a , P.L. Dawson a a Department of Food, Nutrition and Packaging Sciences, Clemson University, Clemson, SC 29634, USA b Prestage Department of Poultry Science, North Carolina State University, Raleigh, NC 27695, USA article info Article history: Received 23 April 2014 Received in revised form 11 June 2014 Accepted 17 June 2014 Available online 24 June 2014 Chemical compounds studied in this article: Tergitol anionic 7 (PubChem CID: 23665769) Keywords: Salmonella Eggs Egg production Free-range hens Campylobacter abstract The present study was conducted to determine microbiological contamination of free-range and con- ventional chicken eggs produced under controlled conditions. Eighty-four certified Salmonella-free Bovan Brown chicks (age 2 days) were grown in 6 separate floor pens until age 16 weeks, and then moved into 3 conventional battery cages (BC) or 3 free-range (FR) housing systems. Total aerobic mi- croorganisms and Enterobacteriaceae on egg shell surfaces were enumerated weekly when the hens were 20e27 weeks of age (N ¼ 535 and N ¼ 541 for BC and FR, respectively). Prevalence of Salmonella and Campylobacter were determined on crushed egg shells (N ¼ 212 and N ¼ 176, respectively) and in feces (N ¼ 36 and N ¼ 30, respectively) collected from hens at 24 and 28 weeks of age. Counts of total aerobic microorganisms recovered from BC and FR eggs ranged from 5.0 to 6.0 log 10 CFU/mL. Numbers of Enterobacteriaceae averaged 1.0 log CFU/mL higher (90% greater) on FR eggs than on eggs from BC hens. Salmonella was not detected on any of the eggs collected from BC hens (0/212), but prevalence on eggs collected from FR hens was 2.36% positive (5/212). Prevalence of Campylobacter recovered from eggs collected from FR (26.1% positive or 46 out of 176 positive) was significantly higher (P  0.0001) than the prevalence of Campylobacter recovered from eggs from BC hens (7.4% positive or 13 out of 176 positive). These data demonstrate that FR eggs, where hens have more contact with eggs after oviposition, have greater microbiological contamination on the egg shell surface than eggs produced in the BC cage systems. © 2014 Elsevier Ltd. All rights reserved. 1. Introduction Consumer emphasis on the humane treatment and environ- mentally friendly production of eggs has influenced U.S. egg pro- ducers to expand into alternative markets, transitioning from conventional battery cage housing systems to free-range produc- tion. Moreover, the European Union (EU) issued the Council Directive 1999/74/EC in 1999 stating that member states should not house laying hens in conventional battery cages after January 2012 (European Commission, 1999). Eggs produced in alternative sys- tems are of interest to the U.S. industry because they demand premium pricing and potentially higher profit to egg producers; however, little is known about the microbiological challenges associated with alternative production practices in the U.S. Previous studies examining differences in microbiological contamination levels between conventional and alternative egg production systems have reported conflicting results (De Reu, Grijspeerdt, Heyndrickx, Uyttendaele, & Herman, 2005a; De Reu et al., 2005b, 2009; Huneau-Salaun, Michel, Huonnic, Balaine, & le Bouquin, 2010; Jones, Anderson, & Guard, 2012; Jones, Anderson, & Musgrove, 2011; Messelhausser et al., 2011). In a controlled experimental setting, De Reu et al. (2005a, 2005b) found that levels of total aerobic microorganisms on eggs collected from an aviary housing system (5.5e6.0 log CFU/mL) averaged approximately 90% higher than numbers of total aerobic microorganisms recovered from eggs produced in conventional or furnished cage systems (3.8e4.6 log CFU/mL). However, when these same researchers conducted a similar experiment in a commercial setting, the number of total aerobic microorganisms recovered from eggs collected from non-caged systems were only slightly higher (4.98 log 10 CFU/egg shell) than numbers on surfaces of eggs from furnished cage systems (4.75 log 10 CFU/egg shell; De Reu et al., 2009). Huneau-Salaun et al. (2010) found similar but less pro- nounced differences when they compared numbers of total aerobic microorganisms recovered from eggs laid in ‘on-floor’ housing systems as compared to counts recovered from eggs laid in * Corresponding author. Tel.: þ1 864 656 3397. E-mail address: jknorth@clemson.edu (J.K. Northcutt). Contents lists available at ScienceDirect Food Control journal homepage: www.elsevier.com/locate/foodcont http://dx.doi.org/10.1016/j.foodcont.2014.06.038 0956-7135/© 2014 Elsevier Ltd. All rights reserved. Food Control 47 (2015) 161e165