Elsevier

Microbial Pathogenesis

Volume 105, April 2017, Pages 340-345
Microbial Pathogenesis

Prevalence, molecular and antimicrobial resistance of Salmonella isolated from sausages in Meknes, Morocco

https://doi.org/10.1016/j.micpath.2017.02.042Get rights and content

Highlights

  • Salmonella was detected in 34 of the 156 samples (21.79%).

  • 4 serogroups and 12 serotypes were identified; Salmonella Corvallis and Salmonella Kentucky were most prevalent.

  • Multidrug resistance was found among the 15 (44.12%) Salmonella isolates.

  • The “ACSSuT” penta-resistance pattern was observed in tow strains of the Salmonella typhimurium.

  • The resistance to Ofloxacin was observed in 4 strains of the Salmonella Kentucky.

Abstract

Salmonella is among the most important food borne pathogens worldwide contaminating a wide range of animal products including meat products. The aims of this study go through two steps: The first step is to estimate the proportion of sausages products contaminated with Salmonella in Meknes city (Morocco), which were collected from various shopping sites: butchery, street vendors, supermarket and souk (Weekly market combines the population of the small villages around Meknes city). The second one is to identify serovars, to determine the antimicrobials resistance patterns of isolates and to detect the invA and spvC genes. 34 (21.79%) Salmonella were isolated, recovered 4 serogroups and 12 serotypes. The most prevalent serotypes were Salmonella Corvallis (23.53%) and Salmonella Kentucky (17.65%). All Salmonella isolates were tested for their susceptibility to 18 selected antimicrobials agents, of which 100% were resistant to at least one antimicrobial, 85.30% (29/34) were resistant to two or more antimicrobials and 44.12% (15/34) were resistant to at least three antimicrobials. All Salmonella are resistant to ampicillin, 76.47% to streptomycin, 20.59% to sulfonamides, 17.65% to Tetracycline and 11.77% to Ofloxacin. The “ACSSuT” penta-resistance pattern was observed in tow of the Salmonella Typhimurium strains. In addition, this study showed that all Salmonella strains (34) were positive for invasion gene invA and negative for the virulence gene spvC.

Introduction

Food-borne diseases imposes a substantial economic burden and threatens the public health on society causing an acute morbidity and chronic sequelae [1], [2]. Worldwide, the consumption of contaminated food is responsible for two million deaths per year [3]. Furthermore, the non-typhoidal Salmonella is the main cause of food-borne diseases, which pose a big problem for medicine and agribusiness; it's associated in most cases with the consumption of animal products [4], [5]. However, some studies show that even of plant origin may be a vector for transmission of Salmonella to humans [6], [7].

Worldwide, Salmonella is responsible for the millions cases of foodborne diseases each year [8]. The incidence of salmonellosis ranged between 14.53 and 17.55 cases per 100,000 people in the United States [9]. Moreover, Salmonella was the second most commonly reported zoonoses in the European Union with a total of 91,034 confirmed cases of human salmonellosis in 2012 [10]. The true incidence of salmonellosis in both humans and animals is difficult to evaluate in developing countries because of the lack of epidemiological surveillance systems [11]. The bacterial resistance to antimicrobial agents, including Salmonella is a major problem of food safety; it affects both the veterinary and public health by transfer of resistant strains to humans through the food chain [12], [13]. The multi-resistant strains can sometimes be the cause of international outbreaks raising fears therapeutic impasses and increased morbidity and mortality for simple food poisoning [4].

In Morocco, the consumption of meat products has experienced a sharp increase in recent years and the presence of Salmonella in these products is usual [14], [15], [16], which increases the population exposure to the pathogenic agent. Also, the manufacture of sausages is done under conditions that do not comply with good hygiene practices. In Meknes city, sausages are sold in supermarkets, butchery, street vendors and souk. The street vendors are located mainly in neighborhoods, they have generally a very low cultural level and are unconscious of good hygiene practices and work in illegal conditions without control and without regulatory legislation. As regards the souk, sausages are presented on parts in contact with air and dust at ambient temperatures, without any respect for good hygiene practices. Those who make a deadly food and a potential transmission vector of pathogenic bacteria to humans.

The aim of this study is to determine the prevalence of Salmonella in sausages made from beef meat, turkey meat and artisanal sausages “Merguez” trades in Meknes city (Morocco), using the conventional method, by biochemical and serological means. The molecular identification by PCR was performed to detect the invA and spvC genes. The sensitivity and resistance of Salmonella to antimicrobials agents were studied. It should be mentioned that “Merguez” is a small raw sausage generally made of lean and fat beef mixed with condiments and stuffed into natural casings of sheep and beef; it is generally sold in street vendors.

Section snippets

Samples collections

From March 2014 until February 2015, 156 samples of sausages (60 of Turkey sausages, 60 of Beef sausages, 36 of Artisanal sausages “Merguez”) were collected from various sites: 72 from butchery, 36 from street vendors, 24 from Supermarket and 24 from Souk (Weekly market) in Meknes city in Morocco, with a frequency of 13 samples per month (5 of Turkey sausages, 5 of Beef sausages, 3 of Artisanal sausages “Merguez”). The collected amount of each sample of sausage is about 40 g, which they were

Prevalence of Salmonella in sausage samples

Salmonella was detected in 21.79% (34/156) of samples. Artisanal sausages “Merguez” are the most contaminated 30.55% (11/36), followed by Turkey sausages 23.33% (14/60) and Beef sausages 15% (9/60). Considering the area of marketing, sausages sold in Street Vendors are the most contaminated (30.55%), followed by souk (29.16%), butchery (18.05%) and supermarket (12.5%). Invasion gene operon invA was detected in all Salmonella isolates in this study. However, spvC was not detected in any strain (

Discussion

The prevalence of Salmonella in sausages is 21.79% (34/156). It's in agreement to those reported in Brazil (24.4%) [19] and Botswana (26%) [20]. However, this value is less than that found in Algeria (46.77%) [21] and higher than that found in Morocco (0.097%) [6] and Italy (3.5%) [22]. A study done in Tunisia showed the absence of Salmonella in Merguez sausages [23]. This comparison should be made with suspicion, because the results may be influenced by several factors such as the level of

Conclusion

In this study, the high levels of contamination of sausages with Salmonella and the detection of several serotypes highlight the poor hygiene all along the chain of manufacture and sale of this product. Furthermore, our results indicate the widespread presence of Salmonella strains resistant to antimicrobials: the resistance of Salmonella Typhimurium “ACSSuT” and the resistance of Salmonella Kentucky to Ofloxacin. So it's time to monitor, control and rationalize the use of antimicrobial agents

References (44)

  • Y. Li et al.

    Salmonella isolated from the slaughterhouses and correlation with pork contamination in free market

    Food control.

    (2016)
  • M. Murgia et al.

    Antibiotic resistance determinants and genetic analysis of Salmonella enterica isolated from food in Morocco

    Int. J. Food Microbiol.

    (2015)
  • A. Adesiyun et al.

    Resistance to antimicrobial agents among Salmonella isolates recovered from layer farms and eggs in the Caribbean region

    J. Food Prot.

    (2014)
  • X. Yang et al.

    Prevalence, antimicrobial resistance and genetic diversity of Salmonella isolated from retail ready-to-eat foods in China

    Food control.

    (2016)
  • F. Adzitey et al.

    Prevalence and antibiotic resistance of Salmonella serovars in ducks, duck rearing and processing environments in Penang, Malaysia

    Food Res. Int.

    (2012)
  • W. Oueslati et al.

    Prevalence, virulence and antibiotic susceptibility of Salmonella spp. strains, isolated from beef in Greater Tunis (Tunisia)

    Meat Sci.

    (2016)
  • R. Nayak et al.

    Genetic diversity and virulence gene determinants of antibiotic-resistant Salmonella isolated from preharvest Turkey production sources

    Int. J. Food Microbiol.

    (2004)
  • J.F. Gruber et al.

    Evaluation of U.S. Poison center data for surveillance of foodborne disease

    Foodborne Pathog. Dis.

    (2015)
  • World Health Organization

    World Health Day: Food Safety

    (2015)
  • X. Kuang et al.

    Serotypes and antimicrobial susceptibility of Salmonella spp. isolated from farm animals in China

    Front. Microbiol.

    (2015)
  • B. Bouchrif et al.

    Prevalence and antibiotic-resistance of Salmonella isolated from food in Morocco

    J. Infect. Dev. Ctries.

    (2009)
  • R.L. Bell et al.

    Ecological prevalence, genetic diversity, and epidemiological aspects of Salmonella isolated from tomato agricultural regions of the Virginia Eastern Shore

    Food Microbiol.

    (2015)
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