Prevalence of Intestinal Parasitic Infections and Associated Factors Among Food Handlers in Wolaita Sodo University Students Caterings, Wolaita Sodo, Southern Ethiopia: A Cross-Sectional Study

Background: Intestinal Parasitic Infections (IPIs) are among the most prevalent diseases in the world, particularly in developing countries with low socio-economic and poor living conditions. From the estimated one third global population infected by intestinal parasitic infections; the majority lives in tropical and sub-tropical parts of the world. These diseases are highly prevalent in Ethiopia. However, its magnitude in the context of Wolaita Sodo University, where a large number of students reside in a campus is not studied. Therefore, the objective of this study was to assess the prevalence and factors associated with intestinal parasitic infections among food handlers in students' caterings of Wolaita Sodo University, Southern Ethiopia. Methods: Institutional based cross sectional study was conducted among food handlers working in Wolaita Sodo University students' caterings' from January 10 to February 10, 2016. The study was undertaken among 233 food handlers by using simple random sampling technique. Data were collected using structured and pretested questionnaire; observation of food handlers while working and microbiological laboratory investigations. Bivariate and multivariate analyses were used to assess the association between covariate and the outcome variables. Adjusted Odds Ratio (AOR) with 95% confidence interval (CI) was considered to ascertain the significance of the association. Results: The mean age of the study participants was 27.2 (±6.4 SD). The overall prevalence of intestinal parasitic infections was 23.6%, with 95% CI of 18.2% to 29.1% of which 12.4% was due to amoeba cyst. Untrimmed fingernail with AOR (95% CI) 2.06 (1.06, 4.00) and regular hand washing habit without soap before food handling with AOR (95% CI) 2.68 (1.25, 5.73) were found to be significantly associated with intestinal parasitic infections. Conclusions: The prevalence of intestinal parasitic infections was high among Wolaita Sodo University food handlers. Untrimmed fingernail and hand washing habit without soap before food handling were found to increase odds of intestinal parasitic infections. The university may need to consider interventions recommended accordingly.


BACKGROUND
Intestinal Parasitic Infections (IPIs) are among the most prevalent diseases in the world, particularly in developing countries with low socio-economic and poor living conditions. (1)(2)(3)(4). From the estimated one third global population infected by intestinal parasitic infections; the majority lives in tropical and sub-tropical parts of the world (5,6). These infections are endemic in some countries of Africa, Southeast Asia, South America and Eastern Europe (2,4,7).
Ethiopia is one of the countries in Africa with high prevalence of intestinal parasitic infections. Based on the studies conducted in Ethiopia; one third of the population is estimated to be infected with Ascaris lumbricoides, one quarter is infected with Trichuris trichiura and one in eight lives with hookworm (4,11,(13)(14)(15)(16)(17). Thus, Ethiopia has the second highest ascariasis, the third highest hookworm, and the fourth highest trichiuriasis infections in Sub-Saharan Africa (4,11,(13)(14)(15)(16)(17).
The health status and hygienic practices of the food handlers are the major determinants of food contamination in developing countries where there is a poor regulatory system for food hygiene. Because of urbanization and expansion of large institutions; eating and drinking from food caterings are becoming common practices in developing countries like Ethiopia (4)(5)(6)11). Often, food handlers in developing countries, including Ethiopia are employed without proper screening for hygiene related infectious diseases (4,11,18). The rapid growth of public universities in Ethiopia in the past two decades, urging to ensure hygienic food handling and preparation practices to safeguard the health of students getting food and drink services in a mass. local studies conducted among food handler's revealed high prevalence of IPIs and unsatisfactory practices of food hygiene measurements (19). However, most studies were old and no similar studies had been conducted in the study area. Therefore, this study aimed at assessing prevalence and factors associated with IPIs among food handlers in the context of Wolaita Sodo University (WSU).

Study Setting and Period
Institutional based cross sectional study was conducted at WSU, Wolaita Sodo, Southern Ethiopia from January 10 to February 10, 2016. WSU enrolled a total of 11,235 regular students in the 2016 academic year in its two campuses located at Sodo town. The university supplies, food and drink services for its students residing in two campuses located in Wolaita Sodo town. There are 558 food handlers working in the students' caterings, of which 144 were males and 414 were females. WSU has only two campuses (Gandaba and Ottona) only.

Source Population
The source population was all food handlers who were working in the students' Caterings of WSU located in Wolaita Sodo town.

Study Population
The study population was randomly selected food handlers working in the students' caterings of WSU. Food handlers engaged in food preparation, serving and cleaning regardless of their employment status were included in the study. Whereas, those who were on annual leave during the data collection time and those who were taking anti-parasitic drugs in the past two to three weeks prior to the data collection were excluded from the study.

Sample Size and Sampling Technique
The sample size was calculated based on a study in Mekelle university showed that IPIs has been reported in 49.4% of food handlers. Assuming, 95% Confidence Interval (CI), 5% margin of error and 10% non-response rate using single population proportion formula, finite population correction factor for a population <10,000 was used to calculate final sample size (19). Hence, a total of 251 samples were determined. Study participants were selected using simple random sampling technique after entering alphabetic ordered lists of food handlers into Statistical Software for Social Sciences (SPSS) version 20. The samples were distributed between two campuses proportional to their size.

Data Collection Instruments and Procedures
A structured and pretested questionnaire was used to collect data related to socio-demographic, economic, personal and environmental characteristics. Variables such as age, sex, monthly income, personal hygiene, regular medical checkup, waste management and accessibility to safe water supply were included in the questionnaire. The questionnaire was prepared in English and translated into local language. Data were collected by two Environmental Health Officers who speak the local language. Trained staffs collected the data. Training for data collectors and supervisor was given for 3 days. Supervision was made by Environmental Health Officer who has experience of research work and familiar with the study area. Pretest before the actual data collection was carried out on food handlers working at Wolaita Sodo Agricultural Vocation Training College with a size equivalent to 5% of the study subjects.
The stool collection and microscopic investigation were conducted by three Medical laboratory technologists. Triplicate smears from the collected sample of every study subjects were prepared. To ensure consistency of measurements every smear examination was carried out and confirmed by two laboratory technologists. Stool specimens were collected from food handlers with labeled wide-mouthed clean plastic cups using clean wooden applicator stick at WSU Teaching and Referral Hospital Medical Laboratory (20,21). From each study subjects about 2 gm of stool was collected. The stool samples were processed in WSU Teaching and Referral Hospital Medical Laboratory using WHO standard and calibrated instruments with a direct microscopic technique to detect cysts, trophozoites, eggs, and larva of intestinal parasites (20). Stool examinations were performed using the formol-ether concentration technique. Both the 10× and 40× objectives were used to detect eggs and larvae of helminthes and cysts and trophozoites of protozoan parasites. Iodine solution was used to detect and identify cysts of protozoan parasites (20,21). The results of the stool examination and observation of the working environment were recorded using checklists.

Data Analysis
Data were checked for completeness and consistency. Coded data were entered using EpiData version 3.1 software and exported to SPSS version 20 for Windows (SPSS, Chicago, IL, USA) for cleaning and analysis. Descriptive summaries were calculated to determine the prevalence of intestinal parasitic infections. Positive result of IPIs coded = 1 and negative results coded = 0 in a logistic regression analysis. Based on the existing evidence, the least contributing factor to the dependent variable was used as reference category. Variables with P-value <0.25 in bivariate analysis were included in the multivariate analysis. Adjusted Odds Ratio (AOR) with 95% CI was considered to ascertain the significance of the association at p-value < 0.05.

Personal Hygiene Practices of Food Handlers
From the total food handlers 113 (48.5%) observed using an outer protective coat or gown during observational assessment of food handlers at work. During observation of finger nail status, 103 (44.2%) food handlers found to have their fingernails untrimmed. About 158 (67.8%) food handlers washed their hands after toilet with soap, while the rest washed only with water. The magnitude of hand washing with soap habit before food handling was 189 (81.1%) ( Table 2).

Knowledge of Food Handlers
Out of the total participants interviewed for knowledge assessment, 225 (96.6%) knew about person to person transmission of IPIs. On the other hand 232(99.6%) knew washing hands before handling food reduce the transmission of IPIs ( Table 3).

Factors Associated With Intestinal Parasitic Infections
Socio-demographic and hygiene related factors such as work experience and finger nail status were entered into binary logistic regression and then variables showing p value <0.25 were re-entered into multivariate logistic regression to control for confounding. From the binary logistic regression analysis, hand washing habit with soap before food handling with Crude Odds Ratio (COR) (95% CI) of 2.84 (1.41-5.72) was positively associated with intestinal parasitic infections. However, in the binary logistic regression variables such as work experience, finger nail status, educational status, hand washing habit with soap after touching dirty materials, nail painted and cleanness of outer garments were not associated with intestinal parasitic infections ( Table 5).
On multivariate analysis hand washing habit with soap before food handling and finger nail status showed a significant association with intestinal parasitic infections. There is a 93 % increased odds of developing intestinal parasitic infections among food handlers who had untrimmed finger nail with AOR (95% CI) of 1.93 (1.01, 3.67). Food handlers who had no habit of washing their hands with soap before food handling were 2.67 times more likely to be infected with intestinal parasitic infections than their counterparts with AOR (95% CI) of 2.67 (1.11, 6.42) ( Table 5).
The rate of double infections was 0.8%. This is relatively similar to the findings from Arba Minich University students' caterings in Southern Ethiopia (0.6%) (16) and Gondar University students' caterings(1.6%) in North-western Ethiopia (24). While it is lower than the finding from Mekelle university students' caterings(5.2%) in Northern Ethiopia (19). Availability and accessibility of medical checkups at Wolaita Sodo University and socio-demographic features might be some of the reasons for the difference.
In this study, the predominant parasitic infection was Amoeba cyst with a prevalence of 12.4%. This is consistent with the finding from Bahir Dar, North-western Ethiopia, 10.2% (29,30). The prevalence of hookworm was 1.3%, which is in consistent with the findings from Jimma, Southwestern Ethiopia (2.9%) (31), and Addis Ababa University (2.1%) (20).
Untrimmed fingernail and hand washing habit without soap before food handling were found associated with IPIs. This is similar with the findings from Arbaminch University; where, untrimmed finger nail, hand washing practice after toilet and hand washing before food handling were identified as predictors for IPIs (16). This evidence also supported with the study conducted from Mekele University; where, hand washing habit with soap before food handling and utilization of soap were found determinants for IPIs (19). Both of the study, participants were from university cafeteria food handlers. In either of evidences, untrimmed fingernail can serve as a vehicle for the transmission of intestinal parasitic infections and washing hands with soap before handling food could remove parasites. The study from Addis Ababa University has found no association between untrimmed finger nail and hand washing habit with soap before food handling; and intestinal parasitic infections (20). Examination of food handlers' fingernail contents for ova or parasites is one way of identifying possible contamination of food; however, the current study did not include the assessment of parasite in the fingernail contents. The data of this study are limited to Wolaita Sodo University; therefore, we recommend further study that include other universities in the country. Since the study, design is crosssectional; it cannot establish temporal relationship between variables; therefore, we recommend intervention study in the same population.

CONCLUSIONS
The present study demonstrated a high prevalence of IPIs among food handlers working in Wolaita Sodo University. The study revealed that fingernail determines the prevalence of IPIs, similarly handwashing with soap before food handling was additional determinants of IPI in food handlers. It identified fingernail status and hand washing habit with soap before food handling as determinants of IPIs among food handlers in Wolaita Sodo University. Therefore, enforcement of standard hygienic and sanitary practices by the university was recommended to improve personal hygiene of the food handlers and sanitary facilities of the caterings.

ETHICS STATEMENT
The study was conducted after obtaining ethical clearance from WSU College of Health Sciences and Medicine institutional ethical review committee. Letter of cooperation obtained from the university was submitted to the students' caterings administration. Informed oral consent was obtained from the participants of the study. Participants found positive for intestinal parasitic infections were treated at WSU Teaching and Referral Hospital. Information obtained from the study participants was kept confidential. Information's were kept locked in office. Any personal information never pass to the third party.

AUTHOR CONTRIBUTIONS
WK, WM, and AA designed the study, responsible for supervision, and wrote the manuscript. WM collected data and analysis.

FUNDING
The research was partially funded by the Wolaita Sodo University.