Introduction

Ready-to-eat (RTE) cold cuts and sausages are foods of great acceptance due to their organoleptic attributes and practicality of consumption. In Mexico, the per capita consumption of these products is increasing, since it is estimated that in 2014, 6.9 kg per person were consumed, while for 2018 the figure increased to 8.1 kg¹. However, the nature and the production of cold cuts and sausages render these foods vulnerable to contamination by microorganisms that cause their deterioration, as well as by pathogens associated to foodborne diseases (FBD)². Listeria monocytogenes is considered the main cause of withdrawal of cold cuts and sausages from the market in the USA.^3-6, and one of the main etiological agents of FBD, with a mortality rate of up to 30 % in certain high-risk groups (immunocompromised, elderly, infants, and pregnant women)^2,4-6. It has been reported as the cause of 1,455 cases (16 % mortality)⁷, with an estimated economic cost of US $ 2.4 billion due to annual listeriosis⁸. However, there are no official references for such estimates in Mexico.

Fortunately, the Mexican Official Norm Project PROY-NOM-213-SSA1-2017⁹, which already establishes the monitoring of this pathogen, has been published. However, because this project is recent, there is little information on the prevalence of Listeria monocytogenes in cold cuts and sausages^10,11. Furthermore, the National Epidemiological Surveillance System does not consider listeriosis as a mandatory notification disease, making it difficult to establish relationships between the presence of the bacteria in food and cases of disease. Even so, the microbiological quality of ham and sausage has already been questioned by the presence of aerobic mesophilic organisms, as well as of pathogenic microorganisms (Salmonella, Staphylococcus aureus)¹². Despite this, there has been no research aimed at establishing the origin of the microbiological contamination of these foods.

In order to guarantee the safety of cold cuts and sausages, the production process adheres to good hygienic practices and to the analysis of dangers and critical control points⁴. In spite of this, poor hygienic handling of these foods in retail stores has been associated as the cause of most reported epidemiological outbreaks⁵.

Several brands of cold cuts and sausages are available in Mexico, which can be sold in bulk or in their original package. In particular, the Mexican consumers’ habit of acquiring cold cuts and sausages in bulk is a worrying aspect, given that it involves handling the food at the point of sale, and violating the brand's quality guarantee. Consequently, the population most affected is the one that seeks to save resources through this practice, and, in addition, does not go to see a doctor in case of contracting an FBD. Therefore, the aim of this study was to generate information on the influence of the type of sale on health quality (Salmonella, Escherichia coli, coliforms)^9,13 and the prevalence of L. monocytogenes in cold cuts and sausages traded in the state of Sinaloa, Mexico.

Material and methods

Results

Table 1 shows the microbiological quality of the samples of cold cuts and sausages according to the type of sale and sausage. In general, 42.7 % (41/96) of the sausage samples included in the bulk (69.0 %) and package (17.0 %) category were outside the sanitary specification (<3 MPN/g) (9.13), since the values of quantification for E. coli and total coliforms were in the range of 10 to 2,860 CFU/g. The incidence rate of samples of sausage and ham that did not meet the health specification ranged from 29.2 % (14/38) to 56.3 % (27/48), respectively. Salmonella was not detected in any of the samples analyzed. Additionally, 6.3 % (6/96) of the samples were positive for L. monocytogenes; bulk (8.3 %) vs package (4.2 %). It should be noted that 60.0% (9/15) of the national brands are outside the sanitary specification^9,13, and four of these brands (26.6 %) were positive for L. monocytogenes.

The microbiological quality profiles highlight that the type of sale is an indicator of the assurance of the safety of most brands of cold cuts and sausages (χ2 = 40.0, P= 0.000) (Figure 1) in terms of coliforms, the bulk sale being a microbiological risk factor, mainly in ham. The type of sale did not influence the presence of L. monocytogenes and E. coli (P<0.05) in the samples of cold cuts and sausages. The risk analysis (odd ratio) determined that the sale in bulk increases 11 times the risk of acquiring a non-innocuous sausage, compared to the sale of the product in its original package. Likewise, the risk analysis by type of sausage shows that selling in bulk increases 41.8 and 5.9 times the risk of acquiring ham and sausages of poor microbiological quality, respectively (Table 2). No significance was observed between the risk of obtaining bulk or package products contaminated with L. monocytogenes; however, this risk may increase by 1-3 times if bulk purchase is chosen.

The letters A-O refer to national brands, and the number of samples per brand is in parentheses. The variability of the number of samples per category depended on the availability of the sample.

Figure 1 Classification of microbiological quality profiles of samples of ham (a) and sausages (b) collected from retail services in Mexico, by national brand 

Discussion

The microbiological quality profiles revealed that most of the brands sold in Culiacan, Sinaloa did not meet the sanitary specifications required for their consumption⁹. This indicates the poor hygienic conditions in which some cold cuts and sausages are processed (marks A, B, C, H), and the influence of the integrity of the original packaging during the sale on the microbiological quality. Although primary contamination of cold cuts and sausages may occur¹⁸, their subsequent handling in establishments and at home can increase the pathogenic microbial load^4-5.

In this regard, the violation of the original packaging, the manual handling by the seller, the slicing and cutting, and the use of non-sanitary packaging for the bulk sale of cold cuts and sausages are attributes observed in the study and are pointed out as factors of microbial contamination of food⁵. The detection of L. monocytogenes and the count of coliforms and E. coli in cold cuts and sausages are indicators of the risk of the development of listeriosis and gastroenteritis, since these foods can be consumed without heat treatment prior to their intake. It is important to highlight that these brands are distributed nationally, and that the habit of buying in bulk is a common practice carried out by the Mexican population, which exhibits a potential public health problem.

An equal risk of contamination with L. monocytogenes has been observed regardless of whether the cold cuts and sausages are acquired in bulk or in packaging; this defines the pathogen as a potential contamination hazard at any stage of the food chain. Kurpas et al⁴ agree that the final contamination of meat products by L. monocytogenes occurs at both the processing plant and the point of sale. This is due to the growth characteristics, propagation pathways and reservoirs of L. monocytogenes, as well as to the poor hygiene of the handler, since this bacterium is persistent in conditions related to food processing⁴. Food contamination with L. monocytogenes is one of the most important challenges faced by the meat industry, due to the bacterium's ability to multiply during refrigerated food storage, and to the fact that a contaminated food may be consumed without additional cooking¹⁹. Many studies have reported the presence of L. monocytogenes in cooked, raw, cured, salted cold cuts and sausages, among others^18,20.

Other food safety concerns with regard to L. monocytogenes are virulence²¹ and antibiotic resistance²², both of which are important factors in the severity of listeriosis and the persistence of the pathogen in the processing environment. These phenotypic attributes have also been previously reported in L. monocytogenes strains recovered from certain foods in Mexico^10,11.

Attention should be paid to the detection of L. monocytogenes in cold cuts and sausages sold in Mexico, since the clinical and epidemiological importance of listeriosis in the Mexican population has been previously documented, highlighting the high mortality rate and the severity of clinical manifestations²³. Listeriosis can be present in the form of sepsis, meningitis, endocarditis, miscarriage, localized infections and gastroenteritis²⁴. Additionally, Castañeda et al²⁵ have established the clonal relationship of a strain of L. monocytogenes isolated from chicken meat as a potential etiological agent of listeriosis in Mexico. Since L. monocytogenes is considered a pathogen responsible for ATS⁷, the prevention and intentional control of the pathogen in the food chain is a guideline for minimizing infection by this bacterium.

Since the sale in bulk is an indicator of high microbiological risk of cold cuts and sausages sold in retail stores, attention must be paid to this habit of buying by Mexican consumers, and actions should be designed to help minimize the risk of infection. The high risk of acquiring non-innocuous cold cuts or sausages due to purchase in bulk denotes the continuous exposure of consumers to microbiological hazards, and proposes this fact as a potential cause of the cases of intestinal infections (5,771,681) and food poisoning (38,815) reported annually in Mexico, and whose classification is not defined²⁶. The fulfillment of the regulatory provisions in the sale of these products, and the application of the protocols of good hygienic practices guarantee the safe sale to the consumers^4,9,13. Some studies suggest that sausages must be sold in their original packaging to maintain their production guarantee⁴. Additionally, consumer education on safety issues is an important action for teaching the proper handling of food and minimizing the risk of FBD²⁷.

Conclusions and implications

The high level of microbial contamination and the detection of L. monocytogenes in cold cuts and sausages of different national brands commercialized in bulk or package, is a common indicator of the lack of good hygiene practices in the food chain, and a high risk of acquiring FBD, since they are ready-to-eat products and are distributed throughout the country. For this reason, it is imperative to call the attention of the Mexican authorities to demand the monitoring of L. monocytogenes in cold cuts and sausages, as well as to implement microbial control strategies in the formulation and sale. Finally, consumers are encouraged to choose products in their original packaging to maintain food safety and brand assurance.