Elsevier

Food Control

Volume 72, Part B, February 2017, Pages 244-248
Food Control

Occurrence and characterization of nontyphoidal Salmonella in retail table eggs in Kandy district of Sri Lanka

https://doi.org/10.1016/j.foodcont.2016.04.024Get rights and content

Highlights

  • Table eggs purchased from 100 retail outlets were tested for nontyphoial Salmonella.

  • Fifteen out of the 100, of which 12 shell washings and 3 contents yielded Salmonella.

  • All isolates were reported human pathogenic serovars namely S. Mbandaka, S. Braenderup, S. Corvallis and S. Emek.

  • Need of assuring microbiological safety of table eggs to ensure consumer safety was discussed.

Abstract

Salmonellosis in humans is typically a foodborne bacterial zoonotic disease. In this regard, eggs and egg products contaminated with nontyphoidal Salmonella represent a serious threat to consumers. Eggs are one of the most common sources of animal protein for Sri Lankans but minimum attention is paid to their quality assurance. Except for a few packaged eggs sold under brand names for higher prices, in general, grading, cleaning or cooling is not practised before sale posing a microbiological health hazard to the general public. Hence, the objective of this study was to identify the presence of Salmonella in raw table eggs available at retail outlets in one selected district of Sri Lanka. Eggs were purchased from 100 retail outlets situated in highly populated areas of the district. Samples were tested for the presence of Salmonella in eggshell washings and egg contents, separately. Isolation and identification of Salmonella was performed according to standard methods. The isolates were serotyped and their antimicrobial sensitivity was determined. Salmonella was isolated from the eggs purchased from 15 retail outlets, of which 12 yielded Salmonella from shell washings and three from egg contents. The serovars identified were S. Mbandaka, S. Braenderup, S. Corvallis, and S. Emek. Except one isolate showing resistance to nalidixic acid and another to a third generation cephalosporin, other isolates were sensitive for the tested antimicrobials. According to the results of this study, retail raw table eggs can be considered as an important source of nontyphoidal Salmonella to egg consumers in Sri Lanka.

Introduction

Salmonellosis is an infectious disease of humans and animals caused by the bacteria Salmonella (OIE, 2010, Chapter 2. 9. 9). Among more than 2500 Salmonella serovars, nontyphoidal salmonellae are important foodborne zoonotic pathogens (Hohmann, 2001). Salmonella colonizes in the gastrointestinal tracts of a broad range of animal species. This bacterium can be either host adapted or non-host adapted. The infectious disease in poultry is caused by non motile, typhoidal Salmonella serovars: Salmonella enterica serovar Pullorum (S. Pollorum) and S. enterica serovar Gallinarum (S. Gallinarum). These serovars are highly adapted to the host with little importance in public health (Shivaprasad, 2000). However, non-host adapted serovars can colonize in many hosts including poultry, cattle and swine, and food derived from these species can be contaminated with the Salmonella in any level of farm to fork food supply chain (Forshell & Wierup, 2006).

Comparing to other animal originated food commodities, raw table eggs and egg products are common vehicles for foodborne Salmonellosis in humans (Threlfall et al., 2014). Eggs can be contaminated by Salmonella either through vertical transmission in which organism can enter into newly formulating eggs while eggs are being passed through the reproductive tract of the infected birds or by horizontal transmission where faeces, utensils, pests or handlers contaminate surfaces of eggs after the egg is laid (Gast et al., 2014, Shivaprasad, 2000, Utrarachkij et al., 2012). Although S. enterica serovar Enteritidis (S. Enteritidis) and Salmonella eneterica serovar Typhimurium (S. Typhimurium) are common causes for poultry associated foodborne illnesses in human (Galanis et al., 2006, Hendriksen et al., 2011) outbreaks due to other nontyphoidal serovars such as S. Mbandaka have also been reported (Bäumler et al., 2000, Paine et al., 2014, Scheil et al., 1998). Similarly, recent review by Threlfall and co-workers, using information from published literature and epidemiological databases, has clearly mentioned the importance of serovars other than -S. Enteritidis as a cause of egg-associated Salmonellosis in human (Threlfall et al., 2014).

In Sri Lanka, published evidences on presence of Salmonella in poultry production chain are very limited. According to a study conducted in our laboratory in the year 2008, by testing 128 broiler meat samples representing four provinces of the country, Salmonella contamination was found as 12% (unpublished data). In addition, Liyanagunawardena, et al., 2012 reported that S. Pullorum and S. Gallinarum, are the commonly associated Salmonella serovars in poultry breeder farms in the country. Although many research has been conducted to understand Salmonella-contaminated eggs as a source of foodborne Salmonellosis in developed countries, such studies are scarce in Asian countries like Sri Lanka. Nevertheless, eggs are one of the most common sources of animal proteins for Sri Lankans. Current per capita consumption of eggs in the country is 108 (DAPH, 2014). In Sri Lanka, table eggs are commonly available throughout the country. A few brands of cleaned and pre-packaged eggs are available for higher prices in large supermarkets and also in some retail outlets in main cities. Loose eggs without packaging, stored in wooden crates, often with some packing materials such as hay or paddy husk, is the most common form available in retail outlets. Generally, those eggs are not graded or cleaned before sale and often visible dirt can be seen on the shells of eggs.

Dirty eggs can contaminate the food chain at many stages not only while preparing egg products but also due to cross contamination with other food during storage in the refrigerator and processing in the kitchen which pose the highest risk to humans. There can be contamination of hands and surfaces with Salmonella and other food borne pathogens during food preparation (Carrasco et al., 2012, Gorman et al., 2002, Soares et al., 2012). With the recent trend in fast food systems in the country where food is subjected to less heat and/or prepared in small road side boutiques, the risk due to cross contamination can be significant. Identifying this risk is highly necessary when public health is concerned. In the absence of supporting evidences, such as prevalence of nontyphoidal Salmonella in poultry layer farms or epidemiological data on human Salmonellosis outbreaks due to consumption of eggs in Sri Lanka, this study was aimed at isolating, identifying and antimicrobial resistance profiling of Salmonella serovars present in retail table eggs.

Section snippets

Sampling

Based on the current practices in egg production chain and observations made in the retail outlets in the said district, we hypothesised that considerable number of consumers may expose to potentially pathogenic Salmonella through raw table eggs. Therefore, it was decided to test table eggs available at 100 randomly selected retail shops for the presence of Salmonella.

Kandy district consists of 20 administrative regions called divisional secretariat divisions (DSD) (http://www.kandy.dist.gov.lk

Results

The eggs purchased from 100 different retail outlets (10 eggs from each outlet), which included six pre-packaged eggs belonging to different brands and loose eggs, were tested for Salmonella, both in egg shell washings and egg contents. Of the 200 analyses carried out 15 became positive for Salmonella. Out of 15 samples, 12 yielded Salmonella from shell washings and three from egg contents. None of the samples were Salmonella positive in both the shell washing and the contents. Accordingly,

Discussion

This study indicated a noteworthy level of Salmonella contamination which was 15% in retail raw table eggs in the studied district of Sri Lanka. Even though this is a novel finding to the country, contamination of raw table eggs with Salmonella has been extensively reported elsewhere in the world. In the UK, the reported level of contamination was 0.38% according to a survey carried out in food service premises from 2005 to 2006 (Little et al., 2008). India has reported 7.7% contamination by

Conclusions

Out of the 100 retail outlets, 15 had table eggs contaminated with nontyphoidal Salmonella serovars indicating a potential health risk to public. Contamination of eggshell washings was three times higher than that of the egg contents. The serovars identified were S. Mbandaka, S. Braenderup, S. Corvallis and S. Emek. Occurrence of these serovars raises concern because of their association with reported human illnesses. Except two isolates, one resistant to nalidixic acid and the other to

Acknowledgements

The authors would like to thank Miss. K. Kuruppu and Dr. L. Ranathunga for technical assistance. This work was supported by the WHO Collaborating Centre for Antimicrobial Resistance and WHO Global Foodborne Infections Network (www.who.int/gfn).

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