Identification of drug-resistant Salmonella from food handlers at the University of Gondar, Ethiopia

Infection due to Salmonella is a public health problem both in developed and in developing countries. WHO estimated that, globally 3 million Salmonella associated deaths have been annually reported. Salmonella infection most commonly occurs in countries with poor standards of hygiene in food preparation, handling and sewage disposal [1].

Food borne salmonellosis often follows consumption of contaminated animal products, fruits and vegetables as well as contamination through unclean work surfaces used to prepare foods. Food can also be contaminated by food handlers who do not thoroughly wash their hands with soap after handling raw foods or after using the bathroom. The carrier states of humans are of concern to the food manufacturing and food service institutions because of the risk of contamination of food [2].

The widespread nature of salmonellosis and the spread of antibiotic resistance are of major concern for both developed and developing countries. An example of the global threat of antibiotic resistance is the multidrug-resistant (MDR) Salmonella, resistant for three or more antimicrobial classes. MDR isolates have been widely reported in Europe and America from travelers and adopted children [3]. MDR in both the hospital and community environment are important concern to the clinician, patients and the pharmaceutical industries. Antimicrobial drugs misuse, drugs prescription without susceptibility test, self-medication and long duration of hospitalization was suggested to augment the problem of MDR in developing nations [4].

The true incidence of salmonellosis in humans is difficult to evaluate because of lack of an epidemiological surveillance system in different areas, particularly in developing countries. But a few studies indicated the widespread occurrence and distribution of Salmonella in Ethiopia. According to reports [5–7], in recent years the number of out breaks of Salmonella in humans and its antimicrobial resistance has increased considerably in the country. Despite the challenge, research conducted about food salmonellosis among food handlers and its antimicrobial susceptibility pattern is scarce in Ethiopia particularly in Gondar. Therefore; this research was initiated to determine the prevalence and antimicrobial susceptibility pattern of Salmonella isolates among food handlers working at the University of Gondar students’ dining rooms to recommend appropriate prevention and control measures.

The current study documented that 3.1% of food handlers had Salmonella infection which is consistent with 3.4% reported from Addis Ababa [12] and 2.3% from Ghana [13]. However; this was lower than 7% [14], 13.63% [15], and 18% [16] prevalence from Jakarta (Indonesia), Addis Ababa (Addis Ababa), and Nigeria, respectively. The lower prevalence rate in the present study might be due to the fact that food handlers in University of Gondar had a better habit of hand washing after using a toilet and before handling of food than food handlers participated in other studies aforementioned above.

On the other hand, lower prevalence rates of Salmonella infection were reported from different studies compared to this study. In these reports there were no Salmonella infection among food handlers working in a student’s cafeteria of University of Gondar and Gondar Teachers Training Collage [17], in food workers of Turkey [18], in food handlers at Hawassa [5], and food workers in a medical college in North India [19]. In another studies, 0.93% and 0.03% Salmonella infection rates were recorded from Northern Ethiopia asymptomatic food handlers [20] and amongst food workers in hotels, supermarket, food factories, and restaurants in Japan [21], respectively. The sample size and personal hygiene differences of the food handlers might help to explain this discrepancy.

The high prevalence of Salmonella in the age group of 18–37 years in the present study was comparable with a study conducted in Addis Ababa [12]. This might be due to the fact that the chronic Salmonellae carrier state occurs most commonly among middle age women [22]. In addition, the prevalence of Salmonella infection was higher in females in the current investigation; supported by the previous studies in Ethiopia [12] and Ghana [13].

The results of antimicrobial susceptibility test in the current research revealed that nearly half of (46.2%) the isolates were multidrug-resistant according to the recent drug-resistance definition [23]. In addition, all of the Salmonella isolates were resistant for at least one or more drugs tested. Further analysis of antimicrobial susceptibility test results showed that 69.2% of Salmonella isolates were resistant to Amoxicillin which conform a report from Nigeria [16] that proved Salmonella species in recent years have become progressively more resistant to clinically useful antibiotics including Amoxicillin. The resistant nature of Salmonella isolates to Amoxicillin might be ascribed to high level of utilization of this drug due to its relatively cheaper price and readily available nature to the local community in the current study area. This might create the opportunity for misuse of this drug thus heralding the emergence of resistant strains of Salmonella. Furthermore, 54.8% Salmonellae isolates were resistant to ampicillin. This finding was in agreement with findings from Jimma and Addis Ababa that reported 54%, [6] and 59.4% [7] resistant isolates, in that order. But this ampicillin resistance pattern of Salmonella isolated during this study was lower from reports that indicated 100% [15] and 82.3% [24] resistance in Addis Ababa isolated from dairy farm attendant and pediatric patients, respectively. Furthermore; the current result was lower than 87.5%, 100%, and 91.8% of ampicillin resistant Salmonella isolates reported from Addis Ababa [12], Bahir Dar [25] and Tamil Nadu [26], respectively.

The 46.2% tetracycline resistant Salmonella isolates registered in our research was in agreement with 46.9% [7], but higher than 33.3% [15] resistance reports from Addis Ababa. Yet it is by far lower than 92.9% resistance disclosed from USA [27]. Tetracycline is the most frequently prescribed drug in the current study area including for other infectious diseases both in human and veterinary medicine that could also be mentioned as one of the reasons for the development of such a higher resistance. A worrying aspect of the current result is that it will also be difficult to treat other clinical infectious cases using tetracycline. Although the resistance pattern of Salmonella isolates from food handlers for sulphamethoxazole-trimetoprim in this study is low (15.4%), previous studies have documented much higher [24, 7] and lower [15] resistance rates from Ethiopia in different times.

Interestingly, all of the Salmonella isolates in the current investigation were susceptible to gentamycin and ceftriaxone, which is in agreement with similar studies in Lagos [28] and Ethiopia [12]. This result was higher than 75% [15] and 19.8% [7] susceptibility reports for gentamycin and 78.8% [7] for cetriaxone from Addis Ababa. ceftriaxone is relatively recently introduced and more costly drug compared to cephalothin in the current study area. Due to this, the community might have used it less frequently that contributed for the low rate of resistance recorded. Good efficacy was also observed in nalidixic acid in which 84.6% of the isolates were susceptible that was nearly in line with the study conducted in Lagos, Nigeria [28] and Tamil Nadu, India [29]. In contrast, a study conducted in Ghana revealed resistance to nalidixic at a higher level [30]. These differences to nalidixic acid efficacy might be due to presence or absence of previous exposure of isolates to the drug in other countries than this study area or it might be due to the fact that nalidixic acid is costly and only rarely prescribed in our study area. On the other hand, 46.2% of the isolates exhibited resistance to nitrofurantoin, which is higher than 15% resistance profile reported from Addis Ababa [15].

Drug resistant including multidrug-resistant Salmonella isolates are circulating among food handlers at the University of Gondar posing high risk of infection for the University community having close contact with those carriers. Programmed medical checkup for food handlers with respect to infectious diseases was not practiced at the University. Health education and check-up, and immediate appropriate treatment strategy for positives based on in-vitro antimicrobial susceptibility tests should be in place. Further in-depth serotyping and drug resistant gene identification should be carried out.

Authors are human and animal health professionals and members of Zoonosis and Food Safety research team at the University of Gondar. They are engaged and interested in Zoonotic Food-borne Pathogens and Food Safety research.