Abstract
Background
Salmonella, is among the leading cause of foodborne illnesses in humans, is primarily sourced from food-producing animals. The prevalence of multidrug-resistant Salmonella species has significantly increased in recent years.
Methods
A cross-sectional study was conducted from November 2022 to May 2023 to determine the prevalence and antimicrobial susceptibility pattern of Salmonella in apparently healthy slaughtered cattle and abattoir personnel at Gondar Elfora abattoir. The study was conducted 253 samples in total, including 75 carcass swabs, 75 liver tissue samples, 75 intestinal contents samples, and 14 stool and 14 water samples from the slaughterhouse. Salmonella isolates were identified using standard isolation and identification techniques. Each isolate was also subjected to Kirby–Bauer disc diffusion tests for antimicrobial susceptibility. STATA version 14 was used to compute and analyses various data from slaughterhouses, antimicrobial susceptibility test results, and animal samples using descriptive statistics.
Results
The overall proportion of Salmonella positive isolates was 13.4%( 253/34) in difference sample sources. The prevalence of Salmonella in cattle was 12% (27/225), of which 17.3% were from carcass swabs, 10.7% were from liver tissue, 8% were from intestinal contents, 14.3% were from human stool, and 35.7% were from water samples. Salmonella isolates were resistant to antimicrobials with specific resistance rates 58.82% for cefoxitin (95%Rn: 42.28 – 75.37), 41.2% (95%Rn: 24.63 – 57.72) for ampicillin and 35.3% (95%Rn: 19.23 – 51.36) for tetracycline. Low resistance pattern was reported in chloramphenicol 17.65% and nalidixic acid 14.71%.
Conclusions
The study highlights the high prevalence of Antimicrobial-resistant Salmonella, a significant public health concern, emphasizing the need for effective surveillance, control measures, biosecurity, Mandatory abattoir worker training, and Antimicrobial stewardship in livestock.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12866-025-04262-3.
Keywords: Abattoir, Abattoir workers, Antimicrobial, Cattle, Gondar, Salmonella
Introduction
Foodborne illnesses have become a significant global public health issue in recent years, with implications for both health and the economy becoming more widely acknowledged [22, 26]. The economic impact of foodborne diseases is also significant, with a recent World Bank study estimating that the productivity losses attributed to unsafe food in Africa were 20 billion in 2016, with an additional 3.5 billion spent on treating foodborne illnesses [19]. In countries like Ethiopia, percentage of abattoirs lacking clean water and food handling practices, inadequate food safety regulations, weak regulatory frameworks, limited funding for better equipment, and lack of education for food handlers have all contributed to the widespread occurrence of foodborne diseases [38].
Various pathogens are involved in causing foodborne diseases, with many of them being zoonotic and originating in healthy food animals before spreading to different kinds of foods [11]. Among these pathogens, Salmonella is recognized as the most common foodborne pathogen globally [12, 34], and has long been known as a significant zoonotic microorganism affecting both animals and humans [12]. These pathogens are mainly transmitted through the trade of animals and consumption of raw meat animal products [29]. In slaughterhouses, contamination of carcasses and organs with Salmonella often occurs during meat processing, particularly when the gastrointestinal tract is removed, and there is a risk of spread through cross-contamination by abattoir workers [3].
Salmonella, a member of the Enterobacteriaceae family, is closely related to other significant pathogens such as Escherichia coli, Shigella, and Klebsiella [16]. The genus Salmonella is a common pathogen that can infect a wide range of animals including mammals, birds, fish, reptiles, and humans. Salmonella is divided into two subspecies: enterica and bongori, with enterica being the most prevalent subspecies affecting both domestic animals and humans [37]. There are currently more than 2,700 serovars of Salmonella, which are identified based on antigenic variations in the O (lipopolysaccharide), H (flagella), and Vi (capsular) antigens following the Kauffmann-White scheme [20, 21].
Antimicrobial-resistant Salmonella infections are a major global concern in both humans and animals, especially in developing countries where the risk of infection is high due to poor living conditions, close contact, and shared living spaces between animals and humans [17]. The Antimicrobial overuse in animal production systems has long been suspected as a contributor to the emergence and spread of antimicrobial-resistant Salmonella [7]. Commonly used antibiotics in countries like Ethiopia and other African nations include tetracycline, β-lactams, chloramphenicol, quinolones, nitrofurans, and macrolides [14]. Salmonella is a significant foodborne pathogen worldwide, and infections with Salmonella species are a leading cause of diarrhea in both children and adults [5]. It is estimated that there are 93.8 million cases of gastroenteritis caused by Salmonella each year [26].
Salmonella may be present in cattle and other food animals at the time of slaughter, which could cause contamination and make it possible for food products to become contaminated. This implies that Salmonella can pose major threats to food safety in cattle and slaughterhouse environments, as well as through the potential for carcass and edible organ cross-contamination [37]. Numerous zoonotic Salmonella serotypes are known to be significantly influenced. The two most prevalent Salmonella serotypes linked to cows are Salmonella enterica subspecies enterica serotype Dublin (S. Dublin) and Salmonella enterica subspecies enterica serotype Typhimurium (S. Typhimurium) [33]. The cross-contamination of beef carcass tissue during hide removal and the existence of S. typhimurium in cattle excrement [13].
Studies on the prevalence and patterns of antimicrobial resistance in various regions of Ethiopia highlight the high rate of salmonellosis in the nation and the dangerous resistance of Salmonella species to common antimicrobial agents [1, 15, 25, 27, 35]. However, there are Only 3 studies on the incidence of Salmonella species and patterns of antimicrobial resistance in northwest Ethiopia since 2018–2023. Thus, the current study was to determine the prevalence and antimicrobial susceptibility pattern of Salmonella from apparently healthy slaughtered cattle, and abattoir workers, slaughterhouses and their associated risk factors in Gondar ELFORA Abattoir in Central Gondar zone, Ethiopia.
Materials and methods
Description of the study area
The study was conducted at the Gondar ELFORA abattoir in Central Gondar (Fig. 1). Which is 740 km from Ethiopian’s capital city, Addis Ababa, and northwest of the country. Sheep and cattle are slaughtered at the Gondar ELFORA slaughterhouse. The abattoir slaughters between 10–20 cattle and 5–10 sheep every day, with the animals coming from both rural and urban areas. In the Gondar ELFORA abattoir, there are two veterinary professionals and 15 trained workers who regularly undertake slaughtering activities. Veterinarians perform ante-mortem and postmortem inspections, and reaming activities are carried out by trained workers. There was no clear division of the slaughtering process into stunning, bleeding, skinning, evisceration, chilling, cutting, or frozen delivery in the Gondar ELFORA abattoir. Bleeding and evisceration were conducted in a horizontal position on the floor by incising the hide at the bottom of the abdomen without flying the skin. Workers hoisted the carcass manually via a chained pulley system after flying the skin and eviscerating it on the floor. There were no knife or axe sharpening machines. There were no means of sterilizing equipment, and the carcasses were manually quartered using axes.
Fig. 1.
Map of the study area Gondar ELFORA abattoir. Source: ArcGIS 10.8
Study animals
The study was conducted on 75 apparently healthy slaughtered cattle by using systematic random selected techniques at Gondar ELFORA abattoir from November 2022 to May 2023. The animals originated from different agro-ecological zones with different management systems. The animals were both local and crossbred cattle. The animals sourced from rural areas are kept to graze pasture on grassland and supplementary feedings of crop residue when pasture is scarce, especially during the long dry season. In Gondar town, a semi-intensive management system is used, and the animals are fed with concentrate and hay. The means of transporting animals to the abattoir are by using a car and on their feet. After they were presented to the abattoir, they were kept for an average of 6 h without feed or water in the holding pens. Almost all the slaughtered animals were adult male cattle, and the majority of them had finished traction.
Study design
A cross-sectional study was conducted from November 2022 to May 2023. Systematic random sampling techniques were used to select slaughtered cattle at Gondar ELFORA Abattoir, and abattoir workers were included in the present study regardless of age, breed and sex. Those abattoir workers who started or recently taking antimicrobials during and before stool data collection were excluded from the study.
Sample size determination and sampling technique
The sample size was calculated via the formula recommended for the systematic random sampling technique [36], and an expected prevalence of 4.46% was assumed [24], with 5% desired absolute precision and a 95% confidence interval. The sample size was calculated as follows:
 |
Where N is the required sample size, p is the expected prevalence, and d is the desired absolute precision of 0.05.
A previous study on Salmonella in abattoirs at Addis Ababa, which is an ecologically similar area, revealed an average prevalence of 4.46%. Therefore, using this 4.46% expected prevalence, the calculated sample size was 68 cattle. The number of animals needed to estimate the prevalence of Salmonella in Gondar ELFORA abattoir of the selected town.
The animals were selected via a systematic random sampling technique. Sampling started when the first animal was slaughtered on each sampling day and was continued every three intervals until the animals were slaughtered on a similar day.
Sampling procedure and types
Liver tissue, intestinal contents, and carcass swabs were taken from the systematic random selected slaughtered cattle and stored in a sterile box with ice packs. Following evisceration, liver tissue (more than 25 g) was taken from each of the selected animals. By cutting at both ends with a scalpel blade, intestines conducting roughly 25 g of their contents were collected in sterile universal bottles. Every cut made during sample collection was made with sterile forceps and sterile scalpel blades. The carcass was consistently wiped on both sides from the hindquarter to the forequarters using sterile cotton swabs wet with 10 mL of buffered peptone water (BPW).
The study involved swabbing carcasses with a sterile stick, inserting samples into bottles containing BPW, and collecting them at the end of slaughtering. Samples were labeled and stored in an ice box before being transported to the Microbiology Laboratory, College of Veterinary Medicine and Animal Sciences. Individual stool samples for isolation and identification of Salmonella were collected to check and determine the status of the abattoir workers in sufficient (25 g) aseptically before antibiotic treatment was performed (Annex II).
Water samples used in the abattoirs were collected for isolation and identification of Salmonella accordingly: the tap was opened, and the water was allowed to run for 3 min, followed by the filling of sterile bottles to approximately three quarters full. The bottles containing the water samples were immediately placed in cooler boxes containing frozen freezer packs.
Sample processing
A total of 25 g of liver was weighed, minced, added to 225 ml of BPW and agitated by a homogenizer. Twenty five grams of the intestinal content was weighed on sterile aluminum foil and placed in sterile test tubes. Approximately 225 ml of BPW was added and agitated manually to disperse the content. Each carcass swab was agitated manually while in the original sterile universal bottle containing 10 ml of BPW.
Questionnaire survey
Semi structured questionnaire was used to assess awareness of hygienic practices, and the management system at the Abattoir was assessed and completed by slaughterhouse workers (Annex VI). The questionnaires included the following: (i) slaughterhouse practices (cleaning and disinfection of pens, truck washing, frequency of knife disinfection, water treatment, etc.); (ii) information on the animal (cleanliness of the animals); and (iii) any event during the slaughtering that may have affected the contamination of carcasses (mechanical problems, slaughter rate, condemnation rate, gut ruptures, percentage of filled stomachs, use of treated water for carcass washing and employee training).
Practical observation of Gondar ELFORA abattoir company
Gondar ELFORA abattoir is where cattle and sheep are slaughtered. Animals for slaughter were derived from different areas of Gondar. Approximately 10–20 cattle and 5–10 sheep were slaughtered daily at the abattoir. At the Gondar ELFORA abattoir, there were two veterinary professionals and 15 trained workers who had been performing slaughtering activities regularly. Veterinarians perform antemortem and postmortem inspections, and the remaining activities are carried out by trained meat inspectors.
There was no clear division or room for the slaughtering process; stunning, bleeding, skinning, evisceration, chilling, cutting, or frozen delivery at the Gondar ELFORA abattoir. Bleeding and evisceration were conducted in a horizontal position on the floor by incising the hide at the bottom of the abdomen without skinning the skin. Workers housed the carcass manually via a chained pulley system after they flew their skin and eviscerated it on the floor. There were no knife or axe sharpening machines.
There were no means of sterilizing equipment, and the carcasses were manually quartered using axes. The Gondar ELFORA abattoir Company has two dedicated lines for cattle and Shoat slaughter. It’s Lairage has enough pens for daily slaughtering, but the fasting period is not like the scientifically recommended period, which is 12–24 h prior to slaughtering. Slaughter operations were performed on slaughter lines, including separated wet areas and clean areas. After being stunned in a stunned box via a sharp knife (sticking), the animals were attached to the right rear leg and directly (within 60 s) exsanguinated. Before skining, the head and hooves were detached. Skinning operations include manually performing pre-skinning and mechanized skinning via an upward-pulling hide puller.
Before evisceration, the carcasses were moved into separate clean areas. Evisceration involved slitting the belly, removing the gut and removing the thoracic viscera. The carcasses were then split along the midline from back to front with a splitting saw. After trimming, meat inspection, weighing and grading, the carcasses were washed with cold potable water to remove visual debris. Slaughterhouse workers are not aware of the standard handling of carcasses because their education level is at the elementary level. Postmortem inspection was performed by veterinary doctors after the evisceration process. The average number of cattle slaughtered at the abattoir is 5–20 per day without the eve of ester or holydays.
Isolation and identification
Salmonella isolation and identification were carried out in line with the guidelines of the International Organization for Standardization [23]. Steps that include primary enrichment in non-selective liquid medium (pre-enrichment), secondary enrichment in selective liquid media, plating out on selective media and final confirmation by biochemical tests were employed. The bacteriological media used for the study were prepared according to the manufacturer’s recommendations, as shown in (Annex III).
Isolation
Primary enrichment in nonselective liquid medium (pre-enrichment): During transportation, chilled samples were pre-enriched with an appropriate amount of buffered peptone water and then mixed well. The mixtures were homogenized via a laboratory blender at high speed for 2 min. The enrichments were then incubated aerobically at 37 °C for 18–24 h.
Secondary enrichment in selective liquid media: Rappaport–Vassiliadis medium (RV) broth and Müller Kauffman tetrathionate with novobiocin (MKTTn) broth were used for selective enrichment of the samples. Approximately 0.1 ml of the pre-enriched sample was transferred into a tube containing 10 ml of Rappaport Vassiliadis medium (RV broth) and incubated at 42 °C for 24 h. Another 1 ml of the pre-enriched broth was also transferred into a tube containing 10 ml of MKTTn broth and incubated at 37 °C for 24 h.
Plating and identification
A loop full of inoculums from each RV and MKTTn broth culture was plated onto Xylose lysine deoxycholate (XLD) agar and brilliant green agar (BGA) plates and incubated at 37 °C for 24 h. After incubation, the plates were examined for the presence of typical and suspected colonies. Typically, colonies of Salmonella grown on XLD agar have a black center and a lightly transparent zone of reddish color due to the color change of the media [23].Whereas H2S-negative variants grown on XLD agar are pink with a darker pink center. Lactose-positive Salmonella strains grown on XLD agar are yellow with or without blackening. The typical colonies of Salmonella on BGA are pink, are 1 mm to 2 mm in diameter, and cause the color of the medium to change to red. Five typical or suspected colonies were selected from the selective plating media, streaked onto nutrient agar plates and incubated at 37 °C for 24 h. Isolates that were confirmed as Salmonella were preserved in nutrient broth supplemented with 35% glycerol and stored at −20°C. While the nutrient broth containing Salmonella were monitored daily to ensure their viability for biochemical testing. The pure cultures obtained from nutrient agar and TSA plates were subsequently inoculated into various biochemical confirmation media using an inoculating loop, for subsequent polymerase chain reaction and antimicrobial susceptibility testing (Annex III).
Biochemical tests
Biochemical tests were performed according to ISO-657: 2002 by using different biochemical tests including triple sugar iron agar, lysine iron agar, urea broth, indole tests, and citrate utilization tests, as shown in (Annex IV). These mixtures were incubated for 24—48 h at 37 °C. Colonies producing an alkaline slant with an acid bottom and hydrogen sulfide production at the TSI, positive for lysine, negative for urea hydrolysis, negative for the indole test, and positive for citrate utilization were considered Salmonella.
Antimicrobial susceptibility testing
The antimicrobial susceptibility testing of Salmonella isolates was assessed using the Kirby–Bauer disc diffusion test, which conform to the recommended standard of the Clinical and Laboratory Standards Institute (CLSI, 2019), were used. Antimicrobial susceptibility testing of Salmonella isolates was performed on Mueller‒Hinton agar (Oxoid, England) on the following antibiotic discs with their corresponding concentrations: ampicillin (AMP, 10 µg), tetracycline (TE, 30 µg), cotrimoxazole (SXT, 25 µg), gentamicin (Gen, 10 µg), chloramphenicol (C, 10 µg), norfloxacin (NOR, 10 µg), ciprofloxacin (CIP, 5 µg), cefoxitin (FOX, 30 µg), and nalidixic acid (NA, 30 µg) (Oxoid). Three to five morphologically identical bacterial colonies were suspended in normal saline broth and incubated for 4 h at 37 °C for Growth Promotion, Uniformity, Suspension Medium and Standardization purposes. The bacterial suspensions were compared with 0.5 McFarland turbidity standards. After the turbidity of the inoculum was adjusted, a sterile cotton swab was dipped into the suspension. The swab was streaked onto Muller‒Hinton agar as shown in (Annex V).
The nine commercially available antimicrobial disks were placed on the plate at least 15 mm apart and from the edge of the plates. After the disks were placed, the plates were incubated at 37 °C for 18–24 h. Following incubation, clear zones produced by antimicrobial inhibition of bacterial growth were measured to the nearest millimeter via metal calipers. The diameters of the zones of inhibition were compared with the recorded diameters of the control organism to interpret the strains as susceptible, intermediate or resistant. Antibiotics were chosen on the basis of the prescription practices for Salmonella in this locality and from the literature. An isolate was defined as resistant if it was resistant to one or more of the antimicrobial agents tested, whereas multiple resistances were defined as resistance to two or more antimicrobial agents (CLSI, 2019).
Data management and analysis
All the data were entered into a Microsoft Excel spreadsheet. After validation, the data were imported to STATA version 14 for Windows (Stata Corp., College Station, TX, USA) for analysis. Descriptive statistics such as frequency, percentage, and/or proportion were applied to compute the collected data from different samples of animal origin, abattoir workers, antimicrobial susceptibility test, and the questionnaire survey data results. To identify statistically significant patterns in the data, inferential statistical tests were applied. Specifically, Chi-square (χ2) goodness-of-fit tests were used to determine if the observed frequencies in categorical variables were significantly different from an expected distribution. The threshold for statistical significance was set a priori at p < 0.05. A p-value below this threshold was interpreted as evidence of a statistically significant result.
Results
Demographic characteristics of abattoir workers in Gondar ELFORA abattoir
In the current study, at Gondar ELFORA abattoir, all (100%) of the study human subjects were male, and the majority (66.7%) did not have special training related to meat hygiene (Table 1).
Table 1.
Demographic characteristics of the abattoir workers 2022/20203 (n = 12)
| Variable | Values | Frequency | Percentage (%) |
|---|---|---|---|
| Age (in years) | 18–34 | 6 | 50% |
| 35–49 | 2 | 17% | |
| > 50 | 4 | 33% | |
| Educational status | Informal | 2 | 16.0% |
| Primary | 7 | 58% | |
| Secondary | 1 | 8% | |
| Others | 2 | 16.7% | |
| Duration of job | < 5 years | 5 | 41.7% |
| 5 to 10 years | 2 | 16.7% | |
| > 10 years | 5 | 41.7% | |
| Job type | Carcass processor | 8 | 66.7% |
| Abattoir cleaner | 2 | 16.7% | |
| Meat inspector | 2 | 16.7% | |
| Job relating training | Yes | 4 | 33.7% |
| No | 8 | 66.7% |
Assessment of awareness, hygienic practices, and other factors related to zoonotic links of abattoir workers at Gondar ELFORA Abattoir, 2022/23 (n = 12)
Awareness of Zoonotic Salmonella: The distribution of"Yes"(10) versus"No"(2) is highly unlikely to be due to random chance (p = 0.021). Therefore, Awareness on zoonotic Salmonella is significantly higher than non-awareness. All Other Variables: For all other variables (apron use, hand washing, eating at the abattoir, etc.), there is no statistical evidence to suggest that the split between the two choices is anything other than random chance (Table 2).
Table 2.
Chi-square analysis with the Proportions of awareness, personal hygienic practices and feeding habits of the study abattoir workers (n = 12)
| Variable | Values | Frequency | Percentage (%) | (χ2) | P-value |
|---|---|---|---|---|---|
| Apron (protective clothes) | Used | 7 | 58.3% | 0.33 | 0.56 |
| Not used | 5 | 41.7% | |||
| Wash hands after latrine | Yes | 8 | 66.7% | 1.33 | 0.24 |
| No | 4 | 33.3% | |||
| Manner of hand washing | water only | 8 | 66.7% | 1.33 | 0.24 |
| Use soap and water | 4 | 33.3% | |||
| Eat at the abattoir | Yes | 7 | 58.3% | 0.33 | 0.56 |
| No | 5 | 41.7% | |||
| Eat raw meat | Yes | 8 | 67% | 1.33 | 0.24 |
| No | 4 | 33% | |||
| Aware on zoonotic Salmonella | Yes | 10 | 83% | 5.33 | 0.021 |
Frequency distribution of Salmonella detection in cattle, abattoir workers and water samples
The prevalence of salmonella was assessed an overall salmonella prevalence of 13.4% (95%CI: 9.24% – 17.64%) in different source of sample proportions. And Among the different sources of 225 samples from 75 head of cattle, 12% (27/225) were positive for Salmonella in slaughtered cattle. Since p > 0.05, there is no statistically significant difference in Salmonella prevalence across the three organs (Table 3). Whereas in slaughterhouse samples 14.3% (2/14) stool samples from abattoir workers and 35.7%(5/14) from the tap water. However, No significant difference in Salmonella prevalence between water and stool samples (p > 0.05).
Table 3.
Frequency distribution and chi-square analysis of Salmonella detection in cattle, abattoir workers and water samples in the Gondar ELFORA abattoir
| Organs/source of sample | Examined | Frequency | Percentage | 95%CI | X2 | p-value |
|---|---|---|---|---|---|---|
| Carcass | 75 | 13 | 17.33% | 10.59–27.15% | 3.28 | 0.19 |
| Liver | 75 | 8 | 10.67% | 5.51—19.60% | ||
|
Intestinal content Subtotal (cattle) |
75 225 |
6 27 |
8% 12% |
3.74–16.27% | ||
| Water sample | 14 | 5 | 35.7% | 10.6% –60.80% | 0.76 | 0.38 |
|
Stool sample Subtotal |
14 28 |
2 7 |
14.3% 25% |
8.0% –32.60% | ||
| Over all | 253 | 34 | 13.44% | 9.24% –17.64% |
Antibiotic susceptibility profiles and multidrug resistance patterns of Salmonella isolates
All of the positive isolates obtained from the study (n = 34) were tested for nine different antimicrobials that are commonly used in human and animal treatment and are available on the local market. A total of 31 of the 34 isolates (91.2%) were resistant to one or more of the tested antimicrobials. interpretation standards were used according to CLSI (2019). the isolates were susceptible to the antimicrobial effect of gentamycin (79.4%), amoxicillin/clavulanic acid (61.8%), nalidixic acid and chloramphenicol (58.8%), and ceftriaxone (55.9%). And the isolates also presented high resistance to cefoxitin 58.8% (95%Rn: 42.28–75.37), ampicillin 41.2% (95%Rn: 24.63–57.72), tetracycline and trimethoprim 35.3% (95%Rn: 19.23–51.36) (Table 4 & Fig. 2).
Table 4.
Drug susceptibility patterns of Salmonella strains isolated from cattle and human isolates from the Gondar ELFORA abattoir from November 2022 to May 2023
| Antimicrobials tested | Concentration | Status of antimicrobial against the isolates | 95%(Rn) | ||
|---|---|---|---|---|---|
| Isolates (n = 34) | |||||
| R n (%) | I n (%) | S n (%) | |||
| CX | 30 μg | 20 (58.82%) | 1 (2.94%) | 13(38.24%) | 42.28–75.37 |
| CTR | 30 μg | 8 (23.53%) | 7 (20.59%) | 19 (55.88) | 9.27–37.79 |
| AMP | 10 μg | 14 (41.18%) | 6(17.65%) | 14(41.18%) | 24.63–57.72 |
| AMC | 30 μg | 8 (25.53%) | 5 (14.71%) | 21 (61.76%) | 9.27–37.79 |
| GEN | 10 μg | 5 (14.71%) | 2 (5.88%) | 27 (79.41%) | 2.80–26.61 |
| C | 30 μg | 6 (17.65%) | 8(23.53%) | 20 (58.82%) | 4.83–30.46 |
| NA | 30 μg | 5 (14.71%) | 9 (26.47%) | 20 (58.82%) | 2.80–26.61 |
| TE | 30 μg | 12(35.29%) | 7(20.59%) | 15(44.12%) | 19.23–51.36 |
| TR | 5 μg | 12 (35.29%) | 6(17.65%) | 16 (47.06%) | 19.23–51.36 |
*Rn = resistance
Fig. 2.
Antimicrobial susceptibility, resistant and intermediate test results Legends: CX: cefoxitin, CTR: ceftriaxone, AMP: ampicillin, AMC: amoxicillin, Gen: Gentamicin, C: Chloramphenicol, NA: nalidixic acid, Te: tetracycline, TR: trimethoprim
From a multidrug perspective, the total percentage of isolates susceptible to all drugs was only 8.82%, which means that more than 90% of the isolates were found to be resistant to at least one drug. Among these seven (7) drug susceptible isolates, 50% were found to be resistant to more than three (3) drugs, and 23.53% were found to be resistant to four (4) drugs (Table 5 and Fig. 3).
Table 5.
One or more antimicrobial resistance profiles of Salmonella human and cattle isolates from Gondar ELFORA abattoirs from November 2022 to May 2023
| Resistance level of isolates for MDR test | Freq | % |
|---|---|---|
| All susceptible | 3 | 8.82 |
| One drug Resistance | 7 | 20.59 |
| Two drug resistance | 7 | 20.59 |
| Three drugs resistance | 5 | 14.71 |
| Four drugs resistance | | 8 | 23.53 |
| Five drugs resistance | | 2 | 5.88 |
| Six drugs resistance | | 1 | 2.94 |
| Seven drugs resistance | 1 | 2.94 |
| Total | | 34 | 100.00 |
R0 = susceptible to all; R1, R2, R3, R4 and R5 resistant to 1, 2, 3, 4, 5, 6 and 7 antimicrobials tested, respectively
Fig. 3.
Multidrug resistance test results
Discussion
Salmonella is a significant cause of foodborne disease globally, with its transmission linked to contaminated food and water. The presence of Salmonella in food animals, particularly cattle, poses serious public health risks due to potential contamination of food products [25]. The study found an overall Salmonella prevalence of 13.4%(carcass 17.33%, liver 10.67%, intestinal content 8%, and human stool 35.7%, and water 14.3%). And 12%(27/225) from 75 head of slaughtered cattle in the abattoir. The prevalence reported in the present study was significantly higher than that of reported in other studies (7.6%) in Baher Dar [30]. 4.64% in Addis Ababa abattoir [24], and 4.2% in Deberzite and Addis Ababa [28], in Ethiopia (7.1%) [6]. And This outcome was higher than the Addis Ababa Abattoir's, which reported 9.8% and 11.9%, respectively, Salmonella isolated from cattle [32].
In these studies, three sample types were examined, and a higher percentage prevalence would probably have been obtained if other organs had been examined from the sample types taken from each animal during the study period Carcass swabs, intestinal contents and liver samples proved to be useful indicators of infection, as most bovine Salmonella-positive samples were positive. Healthy carriers typically intermittently excrete only a few Salmonellae [18], unless they undergo some type of stress, such as during transport or holding in the lairage prior to slaughter. The specific prevalence rates of Salmonella in the carcass, liver, intestinal content, stool and water samples collected from Gondar ELFORA abattoirs were 13 (17.33%), 8 (10.67%), 6 (8%), 5 (35.7%) and 2 (14.3%), respectively. The prevalence of Salmonella varied among the sampling organs and slaughterhouse samples. The hypothesis behind this finding is that the prevalence of Salmonella is greater in carcass swabs, liver, and small intestinal contents, as more personnel and meat contribute to cross-contamination. The present findings revealed Salmonella among individuals working in Gondar slaughterhouse samples, including 2/14 (14.3%) from stool samples and 5/14 (35.7%) from water samples.
This prevalence indicates that the study group was composed of carriers of Salmonella with an increased likelihood of infection being transferred to others through contamination with food. Low prevalence of Salmonella in the intestinal contents of bovines in this study supports other findings, indicating that the localization of the organisms in this organ is most likely minimal. The liver is usually free of Salmonella at slaughterhouse, but the surfaces can become contaminated during processing. The ultimate source of this contamination is likely the Salmonella present in the carcass swab and intestinal contents of either the same animal or other animals slaughtered on the same day [31]. This, in turn, implies that the abattoirs used for the slaughtering process, abattoir personnel and butchers could have been contaminated to serve as sources of contamination. The corrective actions required include evaluating cattle cleanliness, improving working procedures/instructions, retraining reviews of cleaning/disinfection materials and maintenance/cleaning equipment, and improving supervision. The possible source of contaminants may be the unhygienic manner of handling meat in abattoirs, the environment upon which the meat is slaughtered, as well as the water [9].
The possible factors that favor the transmission and prevalence of salmonellosis may include environmental and personal sanitation, socioeconomic and living standards, availability of a water supply, and awareness of safe food handling and preparation among individuals. The study suggests differences in hygiene practices at slaughterhouses can significantly impact Salmonella prevalence. Poor hygiene can lead to higher contamination rates, while better practices can reduce the risk of Salmonella transmission from cattle to food products [25]. the present study are greater than those of the other above-listed reports may be due to differences in hygienic and sanitary practices at the abattoirs and sources of animals, types of samples, and sampling techniques. In addition, workers in the current abattoir with poor personal hygiene and a lack of knowledge of the hygienic processing of meat might cause variation. Because it was proven during questionnaire completion that they never had any training regarding the hygienic and sanitation of slaughtering and working environments generally, there was no disinfectant, hot water or separate room for final carcasses and live animals in the abattoir. The overall high level of carcass contamination with Salmonella has special public health significance for a country such as Ethiopia, where raw and undercooked meat is the favorite in most areas [4].
The present study also revealed that 91.2% of cattle and slaughter house isolates were resistant to one or more antimicrobial drugs. This finding is in good agreement with a study conducted in Gondar town on the identification and antimicrobial susceptibility profiles of Salmonella strains isolated from selected dairy farms, abattoir animals and humans. However, the present results were greater than those of a study conducted in Addis Ababa, where 83% of the isolates were resistant to two or more antimicrobials [2]. The current study revealed that gentamicin (79.4%), amoxicillin (61.8%), chloramphenicol and nalidixic acid (58.8%), and ceftriaxone (55.9%), had good antimicrobial activity against both cattle and slaughterhouse Salmonella isolates. This result was comparable with previous reports from animal and human isolates in Addis Ababa [2] and Asela, Ethiopia [10]. However, the present findings contradict those of a study conducted at Jimma University specialized hospital, which revealed that all Salmonella isolates were 100% resistant to chloramphenicol, gentamycin and cephalothin [39]. Another study conducted in Saudi Arabia revealed that 88.6% were resistant to chloramphenicol [8]. The difference in Salmonella antimicrobial resistance levels in different areas of the country may be related to agent risk factors, such as virulence, pathogenicity, infectiousness, and host specificity associated with the genetic composition of Salmonella strains.
The study on Salmonella prevalence in Gondar ELFORA abattoirs has a limitation, including a small sample size, focusing on specific sample types, not systematically analyzing environmental factors, not considering intermittent excretion by carriers, not quantitatively assessing cross-contamination during the slaughtering process, and not evaluating the knowledge and practices of individuals involved in the slaughtering process. These factors could affect the generalizability of the findings and provide insights into the transmission dynamics of Salmonella. Further research is needed to better understand the prevalence of Salmonella in different regions and conditions.
Conclusion
This study highlights a notable prevalence of Salmonella isolates in apparently healthy slaughtered cattle and from various critical control points within the Gondar ELFORA abattoir, including liver tissue, intestinal contents, carcass swabs, stool, and water samples. These findings suggest potential risks for foodborne infections, particularly in areas like Gondar town where raw and undercooked meat consumption is common. Contributing factors may include suboptimal hygiene practices and low sanitary standards within abattoir environments. Moreover, the majority of the Salmonella isolates demonstrated resistance to one or more of the tested antimicrobials, with moderate to high levels of multidrug resistance observed. This may reflect the widespread and possibly unregulated use of antimicrobials in both human and veterinary sectors in Ethiopia. These results raise significant public health concerns, particularly regarding food safety and antimicrobial resistance. However, this study is limited to one abattoir and may not reflect broader regional or national trends. Further large-scale and longitudinal studies are needed to better understand the epidemiology of Salmonella in cattle and its implications for human health, as well as to guide the development of effective interventions and policies for food safety and antimicrobial stewardship.
Supplementary Information
Acknowledgements
The authors express gratitude to the staff in college of veterinary medicine and animal science at the University of Gondar for their unwavering support in this study, Special thanks are also extended to the personnel at the Gondar ELFORA slaughterhouse for their hospitality and invaluable assistance during the sample collection process.
Authors’ contributions
All authors are equally contributed in this study, to the design and writing of the manuscript. Reference managing, data analysis of salmonella circulation in the region, laboratory capacity, and overall review of the manuscript.
Funding
This research was supported by University of Gondar, through the Community service project to the corresponding author. Which was managed by the college of veterinary medicine and animal science from November 2022 to December 2023. The funder had no involvement in the study design, data collection, analysis interpretation, or writing of the manuscript. The authors declare no conflicts of interest related to this financial supporting.
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Declarations
Ethics approval and consent to participate
This study was conducted in accordance with the principles outlined in the Declaration of Helsinki (2013). Informed consent was obtained from all participants prior to their involvement in the study. In addition, it approved by Ethical Review Boards of The University of Gondar (Ref. No. CVMASc/UoG/RERC/17/11/2022) on October 15, 2022. Which were conducted according to local legislation and institutional requirements. Brief information about the purpose of the study and the procedure, risk and benefits of the study was given to the participants via the Amharic language.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
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Supplementary Materials
Data Availability Statement
All data generated or analyzed during this study are included in this published article and its supplementary information files.