Cross-contamination and recontamination by Salmonella in foods: A review

Abstract

The presence of Salmonella in foodstuffs represents an internationally accepted human health concern. Although Salmonella causes many foodborne disease outbreaks, there is little evidence to support cross-contamination as a major contributing factor. However, the paramount importance of preventing cross-contamination and recontamination in assuring the safety of foodstuffs is well known. Sources and factors linked to cross-contamination and recontamination of Salmonella in foods are reviewed in detail. Those foods which are not submitted to lethal treatment at the end of processing or which do not receive further treatment in the home deserves special attention. Salmonella cross-contamination and recontamination episodes have been connected to the following factors: poor sanitation practices, poor equipment design, and deficient control of ingredients. We also examine potential cross-contamination in the home. Cross-contamination and recontamination events at factory level evidence the difficulty encountered for eradicating this pathogen from the environment and facilities, highlighting the need to reinforce industry preventive control measures such as appropriate and standardized sanitation. Also, at consumer level, Public Health Authorities should install hygiene education programs in order to raise consumer awareness of the risks of cross-contamination in the home and their role in its prevention. Finally, a review on cross-contamination models of Salmonella spp. is presented.

Introduction

Salmonellosis represents an important foodborne disease that continues to pose a major and unacceptable threat to human public health in both developed and developing countries (European Food Safety Authority (EFSA), 2010). The dynamics of Salmonella infection is variable and may also be affected by human lifestyle and behavior, changes in industry, technology, commerce and travel (Foley, Lynne, & Nayak, 2008). Salmonella serovars are widespread in nature and can be found in the intestinal tract of all animals species, both domestic and wild (Allerberger et al., 2002) which result in a variety of Salmonella infection sources.

Currently, Salmonella spp. remains a serious foodborne illness risk worldwide according to data (European Food Safety Authority (EFSA), 2010, FAO/WHO, 2002). Salmonellosis accounted for 131,468 confirmed human cases in the European Union (EU) in 2008, representing the second most often reported zoonotic disease in humans following campylobacteriosis. Human salmonellosis cases reported in 2008 show a 13.5% decrease from 2007 in the EU. However, several European countries still show a significant increasing trend, proving that continuous efforts for prevention and control are still necessary.

In the EU, serotypes Salmonella Enteritidis and Salmonella Typhimurium are reported as the two major etiologic agents of salmonellosis that have adapted to humans. In the US, Salmonella Enteritidis and Typhimurium represent the two most frequently reported serotypes according to Centers for Disease Control and Prevention (Centers for Disease Control, 2006). The distribution of Salmonella serotypes in Australia varies geographically. Thus, while S. Typhimurium was the most commonly reported serovar in 2008, S. Enteritidis was frequently reported as cause of human disease, despite it is not endemic in Australia (Yates, 2011). While S. Enteritidis is mostly implicated in the consumption of poultry and eggs, S. Typhimurium is linked to a range of food-producing animals such as poultry, swine, cattle and sheep. S. Enteritidis was a rare serovar until the mid-late 1980s when it emerged as a frequent cause of salmonellosis in European countries and across the globe (Cogan and Humphrey, 2003, Poppe, 1999). By the 1990s, S. Enteritidis replaced S. Typhimurium as the most common serotype of salmonellosis isolated from humans in many countries (Angulo and Swerdlow, 1999, Cogan and Humphrey, 2003, Tschape et al., 1999). Australia and New Zealand, however, experienced a relatively higher number of outbreaks due to S. Typhimurium compared to Canada, the US and the EU (Dalton et al., 2004). Previous salmonellosis outbreaks in Canada and the US have been linked to S. Enteritidis (Centers for Disease Control, 2004). The global distribution of food and the continuous movement of people around the world facilitate the spread of this agent, allowing the introduction of emerging Salmonella serotypes into importing countries.

In general, salmonellosis is transmitted when Salmonella cells are introduced in food preparation areas. Several factors such as multiplication in food due to inadequate storage temperature, insufficient cooking or cross-contamination are often implicated in salmonellosis outbreaks (Ryan et al., 1996, Todd, 1997). The main transmission routes of this pathogen are foods of animal origin contaminated with fecal matter (Haeghebaert et al., 2003, Swartz, 2002). However, consumption of meat from infected animals may also occasionally be a source (Benenson, 1995, Tauxe, 1991).

Some investigations highlight the frequent occurrence of Salmonella in meats and meat products (Mead et al., 1999) Overall, meat, poultry and eggs are acknowledged as constant vehicles of Salmonella serovars and generally involved in the infectious disease (Capita et al., 2003, Wilson, 2002). However, a wide range of other foodstuffs such as milk, dairy products, fruits, vegetables, and fishery products can be sources of Salmonella infection (Todd, 1997). The incidence of Salmonella has been studied in poultry meat in many countries such as the United Kingdom (Plummer & Dodd, 1995), Australia (Fearnley, Raupach, Lagala, & Cameron, 2011), Malaysia (Rusul, Khair, Radu, Cheah, & Yassin, 1996), Greece (Arvanitidou, Tsakris, Sofianou, & Katsouyannopoulos, 1998), Spain (Domínguez, Gómez, & Zumalacárregui, 2001) and Italy (Busani et al., 2005). High prevalence rates have been found in these countries and the serotypes isolated vary geographically with predomination of S. Enteritidis, S. Thyphimurium, S. Hadar, S. Newport, S. Virchow and S. Heidelberg. All these studies emphasize the fact that poultry meat represents a major source of this pathogen and therefore, recontamination of cooked poultry should be considered as a major risk factor. However, the importance and the impact of recontamination events are not frequently well-documented in reports and scientific literature. This lack of supporting evidence may be explained by several reasons, such as incomplete insight in to the causes of foodborne diseases, underreporting cases or lack of outbreak investigation (Reij, Den Aantrekker, & ILSI Europe Risk Analysis in Microbiology Task Force, 2004).

The objective of this review is to examine the role of cross-contamination and recontamination of foods by Salmonella, the principal factors involved, and the strategies developed for prevention of cross-contamination and recontamination.