Salmonella and Shigella carriage among food handlers

ABSTRACT

Background: Food borne diseases have been associated with microorganisms like bacteria, fungi, viruses and parasites. Outbreaks often take place due to the ingestion of pathogenic bacteria. Food handlers are potential carriers of these food borne bacteria. Periodic screening of food handlers can prevent life threatening outbreaks.
Objective: To determine the carriage rate of Salmonella and Shigella spp. among food handlers at a tertiary hospital in Ilorin, North Central Nigeria.
Method: A cross-sectional study that involved screening of all food handlers for specific food borne pathogens was conducted from May to June, 2018.

Finger swabs and fresh stool specimens of the food handlers were collected and specifically examined for Salmonella and Shigella spp. following standard microbiological techniques. Antimicrobial susceptibility testing was performed on all isolates using the Kirby–Bauer disk diffusion method. The socio-demographic characteristics of the food handlers were also obtained using structured questionnaires specifically designed for the study.
Results: Of 81 participants recruited into the study, Salmonella spp was isolated from the stool of 1 (1.

2%) of the food handlers. No Shigella spp. was isolated from the stool cultures. The finger swabs revealed no isolate. The Salmonella isolate was 100% susceptible to Amoxycillin/Clavulanate, Ciprofloxacin, Gentamicin, Ceftazidime and Imipenem.
Conclusion: The colonization rate of food handlers by Salmonella spp. is very low in this study yet epidemiologically significant. Periodic screening and food borne pathogen eradication therapy for infected food borne handlers are recommended to avoid outbreaks of food borne infections in hospitals.
Keywords: Food borne disease, food handlers, food borne pathogens

INTRODUCTION

Food borne diseases (FBDs) are important causes of morbidity and mortality worldwide, especially in the developing nations.

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1FBDs are a serious threat to people in Africa, with a huge public health burden and accompanying massive economic losses.2 According to the most recent World Health Organization (WHO) estimates, 700 000 deaths per year in Africa are due to food and water-borne related diseases. The reported outbreaks only represent the tip of the iceberg, as many more cases that are sporadic have gone unreported.3These diseases have a substantially higher impact in low-income countries and regions with poor water quality, poor sanitation and food safety.4
The microbial agents responsible for FBDs are bacteria, viruses, parasites, and fungi. Food and water are excellent vehicles through which these pathogens can be transmitted to humans. Food borne pathogens (FBPs) can be transmitted at any of the different stages of food preparation which include the farm, the stage of preparation & processing, packaging and distribution. A Food handler (FH) is defined as a person in food trade or someone professionally associated with it, such as a food inspector, who in his or her routine work comes into direct contact with food in the course of production, processing, packaging, or distribution; its procurement, preparation, and consumption.5Food handlers (FHs), with poor personal hygiene and poor knowledge of FBD preventive strategies, working in hospitality sectors or hospitals could spread FBPs and cause deadly outbreaks; thus the health status, personal hygiene, and the knowledge and practice of food hygiene of FHs play important roles in food contamination by FBPs and/or toxins.6
Food borne diseases occur due to the ingestion of bacteria, viruses, fungi or parasites which multiply in the intestine and cause illness or consumption of non-infectious agents like toxins and chemicals.7A common symptom of FBDs is diarrhoea which sometimes is associated with nausea and vomiting. In the hospital setting, nosocomial infection is a common problem that increases the average length of hospital stay and hospital cost and often affects patients’ quality of life, survival, and response to treatment. Poor hygiene of FHs in hospital kitchens has been reported to be the cause of outbreaks of infections in hospitals, some of them resulting in the death of patients.8
Salmonella and Shigella spp. still remain very common bacterial agents of FBDs especially in the developing countries.4These microbes are often transmitted through food, water, nails, and fingers contaminated with faeces. This mode of transmission is referred to as faeco-oral transmission. Hospitalized patients who include pregnant women, infants, the elderly and the immune-compromised persons such as persons with Human immunodeficiency virus (HIV) infection, or individuals on chemotherapy for malignancies are at greater risk of developing FBDs due to their compromised immunity.9
Unsafe food handling and processing can serve as a vehicle for the transmission of a variety of disease causing agents. FHs, who work in the hospital environs, are also potential carriers of agents of FBDs. The potential roles of such FHs in the transmission of food borne infections within hospitals in the Nigeria have not been well elucidated. This study, therefore, determined the prevalence of Salmonella and Shigella spp among apparently healthy FHs at a tertiary hospital in Ilorin, the North Central region of Nigeria.

RESEACRH METHOD AND DESIGN

Study design and area: This was a cross-sectional study that was carried out at the University of Ilorin Teaching Hospital (UITH), Ilorin. It is a hospital with 450 beds and an average of 10,000 and 12,000 annual admissions and Out-patient visits respectively. Ilorin is the capital city of Kwara State, which is located in the middle belt region of Nigeria.
Inclusion criteria: A food handler was defined as a person in the food trade or someone professionally associated with it, such as a food inspector who, in his or her routine work, comes into direct contact with food in the course of its production, processing, packaging or distribution.5All consenting professional FHs, irrespective of their age and gender, were recruited and studied.
Exclusion criteria: FHs who had used antibiotics within one week of recruitment or were still on such drugs were excluded.
Study protocol: The study population comprised 81 FHs and these consisted of the hospital kitchen staff, self employed FHs at the Doctors’ and Nurses’ lounge, and those at the various canteens situated within the hospital premises. An informed written consent was obtained from all the FHs after introducing and explaining the purpose of the study to each of them. Thereafter, each FH completed a structured questionnaire specifically designed for the study. The confidentiality of the FHs was maintained by using codes instead of names and keeping the data away from non-members of the research team.
Sampling technique: Total population sampling was employed and the FHs were recruited consecutively in a non-repetitive manner.
Ethical approval: Ethical approval was obtained from the Ethical Review Committee (ERC) of the hospital before the commencement of the study.
Specimen collection: Finger swabs and fresh stool samples were collected from the FHs over a period of two months spanning between May 2018 and June 2018. The swabs were taken by the researchers, from the inter-digital clefts of the hands and the fingernails of each study participant using a sterile, normal saline-moistened cotton-tipped swab stick. Each swab stick was immediately placed into a labeled sterile bijou bottle containing peptone water before transportation to the laboratory for processing.
Each participant was then given a clean, dry, leak-proof, wide mouthed and well labeled specimen bottle for stool collection. Where the participants could not immediately produce the stool samples, the specimen bottles were left with such participants who were instructed to call any of the researchers on phone as soon as they were about to provide the stool specimen while on duty. The samples were transported to Medical Microbiology and Parasitology laboratory of the hospital within one hour of collection for prompt processing. The socio-demographic characteristics of the FHs were obtained using a structured questionnaire specifically designed for the study.
Laboratory analysis: At the laboratory, all samples were inoculated onto Salmonella-Shigella (S-S) agar and incubated aerobically for 18-24 hours at 35–37 °C.
Handling and processing of finger swab specimens: A flamed and cooled calibrated loop was inserted vertically into the specimen bottle and a loopful of sample was then inoculated on each plate of Salmonella-Shigella (S-S) agar by making a straight line down the center and then a series of close perpendicular streaks throughout the first line. This was followed by fingernail microscopy following the appropriate procedures.10 Handling and processing of the stool specimens: The stool samples were first visually inspected for the presence of blood and/or mucous and worms. Where present, the blood or mucous containing parts of the stool were used for stool wet preparation and inoculation onto the culture medium. Wet stool preparations were made in saline and eosin which were transferred onto slides and microscopically examined under 10X and 40X objectives having applied cover slips on a pre-warmed compound light microscope stage specifically for trophozoites of intestinal parasites. The stool samples were concentrated by formol ether concentration technique and used to identify specifically cysts of intestinal parasites.10 Suspected Salmonella and Shigella colonies obtained after culture were identified with Gram stain reaction, urease test, oxidase test and Analytical Profile Index (API) 20E (Bio Merieux, France). Escherichia coli ATCC 25922 and Staphylococcus aureus ATCC 25923 were used as controls.
Antibiotic susceptibility testing of Salmonella isolates was performed by the modified Kirby-Bauer disc diffusion technique using Mueller-Hinton agar and the results interpreted according to the Clinical and Laboratory Standards Institute (CLSI) guidelines.11Antibiotic discs to which isolates were tested included Amoxycillin/Clavulanate (20/10µg), Ciprofloxacin (5µg), Gentamicin (10µg), Ceftazidime (30µg) and Imipenem (10µg)
Statistical analysis: Data analysis was performed using Statistical Package for Social Sciences (SPSS) version 20. Continuous variables were presented using mean, standard deviation and range. Categorical variables were presented in proportions and percentages.

RESULTS

The ages of the 81 FHs who met the inclusion criteria ranged from 13 to 70 years (mean age ± SD = 37 ± 15 years). Majority of FHs were females 69 (85.2%). The other socio-demographic characteristics of the study population are as shown in Table 1. The hand carriage rate of Salmonella and Shigella spp. among the FHs was 0.0% since none of these organisms was isolated from the finger swabs. Salmonella spp. was however isolated from the stool of one food handler resulting in a prevalence rate of 1.2%. The only isolate was biochemically identified as Salmonella enterica using API 20E (Bio Merieux, France) and it was sensitive to all the antibiotics used for anti-microbial susceptibility testing. No Shigella spp. was isolated from any of the FHs.

DISCUSSION

The age range of the FHs in this study was 13-70 years and it is comparable to that of the kitchen staff in a tertiary care hospital in a similar study conducted in Saudi Arabia.12It however contrasts with the age range of the food service staff in another study in a hospital in Qatar where none of the FHs was less than 20 years of age.13The inclusion of FHs who are not staff of the hospital in this study may account for this observed difference.
In the study from Qatar, unlike in this study, there were more male FHs than their female counterparts with a male to female ratio of 8:1.13Most studies have reported higher proportion of females involved in food handling.14,15 Analyzing the level of education; 49 (60.5%) of the 81 FHs in this study had secondary level of education, and this is at variance with a study in Saudi Arabia where 17 (8.5%) of the FHs has secondary education. Majority of the food handlers in the latter either had no formal education 64 (32.0%) or primary level of education alone 119 (59.5%).12In a study from Qatar, more than 80.0% of the 43 food handlers studied had a minimum of secondary level education.13This percentage is higher than the 60.5% in this study but may be due to the lower sample size in the Qatar study.
Only Salmonella spp. was isolated from the stool of one of the 81FHs in this study giving a total bacteria isolation rate of 1.2%. It is however higher than the rate observed in a similar study of 200 FHs in a tertiary hospital in Saudi Arabia, where neither of the two organisms was isolated from their fingers nor stool.12It is consistent with the range of 0-13.3% reported in a hospital in India over a period of 6 years.16Higher combined stool carriage rates for Salmonella and Shigella spp. ranging from 3.5% and 5.0% in a study from Ethiopia to 35.1% obtained in Nigeria, have been reported among FHs in institutions other than hospitals specifically Universities.17-19Higher carriage rates were recorded among street FHs.4,20,21 This may be due to a better knowledge of FBD and hygienic practice among FHs who work in the health sector than FHs in other institutions and street FHs which has been documented in literature.22
Limitations of the study
Other medically important enteric pathogens such as Campylobacter spp., and Yersinia enterocolitica were not studied due to their challenging growth requirements. Nasal and throat swabs were also not collected and examined for presence of potential food pathogens.

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