Prevalence and factors associated with intestinal parasites among food handlers in Medebay Zana District, North West Tigray, Northern Ethiopia.

DOI: https://doi.org/10.21203/rs.2.23962/v1

Abstract

Introduction

Several epidemiological studies suggest that the prevalence of intestinal parasites is high, especially in developing countries, and are amongst the major public healthchallenges facing Sub-Saharan Africa.The aim of this study was to determine the prevalence of intestinal parasites and its associated factors among food handlers in Woreda Medebay Zana, Tigray, Ethiopia.

Methods

A cross-sectional study was conducted among 401 food handler individuals selected by systematic random sampling.Binary and multivariable logistic regression was used to determine the possible association between the independent variable and outcome variables. Statistical significance was declared at p- value <0.05 with 95% confidence interval.

Result

The prevalence of intestinal parasites was 33.2% within this sample.The dominant parasite were Entamoeba coli 50(37.4%), followed by Entamoeba histolytica/dispar 24(18%), Entamoeba hartmanni 18(13.5), Giardia lamblia 17(12.8%), Schistosoma mansoni 8(6%), Hymenolepis nana 7(5.3%), Enterviousvermicularies 6(4.5%) and Taenia species 3(2.5%).

Conclusion

This study revealed a high prevalence of intestinal parasites among food handlers for a range of intestinal parasites. The significant predictors weresource of water, washing hands before food preparation, washing hands with soap and water after visiting toilet, shower installation, washing body regularly, and eating raw vegetables.

Introduction

Infection with intestinal parasites remains a major public health challenge in developing countries where poor environmental sanitation, poor personal hygiene, and low level of education are prominent[1]. Globally, about one third of the total population is estimated to be infected with intestinal parasites, the majority being people living in tropical and sub-tropical parts of the world [2]. The World Health Organization (WHO) estimated that at least one quarter of the world’s population is infected with soil-transmitted helminthes[3]. Worldwide, about 300 million people suffer from severe helminthic infections, leading to morbidity and over 150,000 deaths annually[4]. The reasons for the incidence of parasites include climatic conditions, local traditions, and the use of human and animal fertilizers in agriculture and vegetable planting[5]. Food sold in markets may be contaminated by hands that have not been washed after defecation or from flies that land on both food and feces, thereby increasing the risk of transmission of intestinal parasites for consumers[6].

Regarding the etiologies, about1.2 billion people were infected with Ascaris lumbricoides, 795 million people with Trichuris trichiura, 740 million people with hookworm, 500 million people with Entamoeba histolytica, and 2.8 million people with Giardia lamblia[7]. As in many developing countries, cases of intestinal parasites are highly abundant in Ethiopia. The country has the second highest burden of Ascariasis, the third highest burden of hookworm, and the fourth highest burden of Trichuriasisin Sub-Saharan Africa[8].

Industrialization, urbanization, and population growth have promoted people to migrate from rural to urban areas, forcing them to have their meals at any place at an affordable price. In urban areas, there is mushrooming of eating establishments due to increased demand with the concomitant. potential to spread of disease via food handlers in those eating establishments[9]. The epidemiology of intestinal parasitesremains complex because of the diversity of associated factors involved, with the complexities of control highly relevant to addressing this escalating challenge [10]. In Ethiopia, particularly in the study area, intestinal parasitosis is a steadily increasing public health concern [11, 12]. Therefore, this cross-sectional study was conducted to assess the prevalence and associated factors of intestinal parasites in food handlers in Woreda Medebay Zana Towns,Tigray, Ethiopia.

Methods And Materials

Study area, design and period

This cross-sectional, community based study was conducted among food handlers working in food service establishments in Medebay Zana Towns from January 2019 to February 2019. Medebay Zana districtis about 1040kms from Addis Ababa. In the district, therewerea total of 277 restaurants and hotels, 44 snack bars and 52 food bakeries. These estalishments can accommodate a total of 1850 people. In total, in the hotels, restaurants and snack bars found in the Woredathere are 1050food handlers.

Population

All food handlers who were working in Woreda Medebay Zana Towns were the source population;randomly selected food handlers formed the study population. Food handlers who wereunder treatmentor who who finishedtreatmentfor parasites within two weeks prior to the study were excluded.

Sample size and sampling technique

The sample size was determined using the following assumptions (level of confidence of the population is taken to be 95% and Zα/2 = 1.96).A 5% margin of error (d = 0.05) and the prevalence of intestinal parasites among food handlers was based on a study done in Ethiopia, Tigray Mekelle Town at 49.3%[11]. Based on these assumptions, the actual sample size for the study is computed using one sample population proportion formula as indicated below.

N = (zα/2) P (1-p)/d

Then, the sample size was, n ≈ 384 + 10% contingency = 422. A systematic random sampling technique was employed to select the study participants from the sampling frame.

Data collection tools

Interviewers administered structured questionnaires adapted from different literatures to collect the data. The content of the questionnaire included socio-demographic characteristics, educational status, economic status, individual behavioral factors, and house characteristics as well as environmental related conditions.

Laboratory Investigation

Fecal specimens were obtained from the selected food handlers and transported to the laboratory based on the standard operating procedures for the collection and transportation of fecal specimens.In the laboratory the stool was immediately examinedby wet mount technique for motile parasites, helminth eggs,cysts, and oocysts of intestinal protozoa followed by Kato-Katz and formol ether concentration technique[13].

Study Variables

Dependent variable: Intestinal parasites status

Independent variable:Socio demographic variables, such asage, sex, monthly income, educational level, service in year; Individual factors, such as poor personal hygiene practice, using fresh vegetable salads and meat, irregular use of sanitizer and disinfectants, poor environmental sanitation, contact with water source, contact with animal, eating raw meat and vegetables; Economic factors, such aspoor quality of housing, poor isolation from work environment when sick, lack of supply of safe water, Lack of access to toilet facility, lack of medical check screening

Data quality assurance

To assure the data quality, the data collection instrument was pretested in nearby towns. Data collectors weretrained before the actual data collection by whom?. Furthermore, the collected data were reviewed and checked for completeness each day. Laboratory investigations were done as per the standard operating procedures for specimen collection, transportation, and analysis of the institution.

Data analysis

After checking for completeness, data were coded, cleaned, and enteredintoSPSS version 21.0 for analysis. Binary logistic regression was used to determine the possible associations between the independent variables and outcome variable.Those factors with p-value of 0.2 and below during the bivariate logistic regression analysis were considered for multivariate logistic regression to control the confounders. Finally, statistically significant was declared at p-value < 0.05 with 95% confidence interval.-

Result

Socio-demographic characteristics

From the total of 422 study participants, 401 wereincluded in this research (95%), of which 377(94%) were females and the mean age of all study participants was 28.74 (± SD = 4.56).From the total participants, 21(5.2%) have completed college and above, 78(19.5%) completed secondary school, 273(68.1%) completed primary school, and the remaining 29(7.2%) were unable to read and write. The study also showed that212 (52.9%) participants had monthly incomes of between 500 and 900 birr and the remaining 189 (47.1%) participants earned ≥ 1000 birr monthly(Table 1).

Table 1
Socio-demographic characteristics of study participants (n = 401) among food handlers in Woreda Medebay Zana (February-March, 2019)
Characters
Category
Frequency
Percent
Sex
Female
Male
377
24
94
6
Age
< 21
21–30
31–40
> 40
28
254
110
9
7
63.3
27.4
2.2
Religious
Orthodox
Muslim
398
3
99.3
0.7
Educational level
College and above
Secondary school
Primary school
Unable to read and write
21
78
273
29
5.2
19.5
68.1
7.2
Monthly income
500–900 birr
1000–1500 birr
212
189
52.9
47.1
Service in year
1–5 year
6–9 year
332
69
82.8
17.2

Hygiene related factors of food handlers

Responses of the study participants showed that 306(76.3%) washed their hands before food preparation, 73(18.2%) washed their hands usually, and 22(5.5%) washed their hands sometimes. Out of the total participants,222(55.4%) washed their hands with soap and water after using the toilet, 378(94.3%) washed their hands after touching dirty materials and different body parts, 180(44.9%) washed their body regularly in their working area, and 284(70.8%) participants had renewed their medical certificate every three months(Table 2)

Table 2
Personal hygiene characteristics of study participants (n = 401) among food handlers in Woreda Medebay Zana Towns (February-March, 2019).
Characters
Category
Frequency
Percent
How often do you wash your hands before food preparation?
Always
Usually
Sometimes
306
73
22
76.3
18.2
5.5
Do you wash your hands by soap and water after visiting toilet?
Always
Usually
Sometimes
222
147
32
55.4
36.7
8
Do you wash your hands after touching dirty materials and d/t body parts?
No
Yes
23
378
5.7
94.3
Do you wash your body regularly in your working area?
No
Yes
221
180
55.1
44.9
Do you have a medical certificate?
No
Yes
0
401
0
100
How frequent do you come to health center for medical checkup?
Every three month
Every six month
Every nine month
284
70
47
70.8
17.5
11.7
Do you wear clean aprons during food preparation?
N0
Yes
137
264
34.2
65.8
Do you wear clean hair garment during food preparing?
No
Yes
122
279
30.4
69.5
How frequent do you cut your fingernails?
Two times per week
One times per week
One times per two week
29
75
295
7.2
18.2
74.1

Housing type and working area related factors of food handlers

From the total of 401study participants, 386 (96.3%) used private tap water, 349(87%) hada shower facility in their working area, 287(71.6%) had separate dressing rooms in their working area, 310(77.3%) used water and detergent to clean utensils and drinking cups, and 87(21.7%) cleaned the kitchen floor at least three times per day (Table 3)

Table 3
Housing type and working area related factors of food handlers (n = 401) in Woreda Medebay Zana Towns (February-March, 2019)
Variables
Category
Frequency
Percent
What is the source of water in your working area?
Private tap
Public tap
386
15
96.3
3.7
Does your working area have shower facility?
No
Yes
52
349
13
87
Does your working area have separate dressing room?
No
Yes
114
287
28.4
71.6
What do you use to clean utensils and drinking cup?
Only water
Water and detergent
Hot water and detergent
53
310
38
13.2
77.3
9.5
How frequently is the kitchen floor cleaned?
One times per day
Two times per day
Three times per day
115
199
87
28.7
49.6
21.7
Do you have toilet facility in your working area?
No
Yes
0
401
0
100

Prevalence and type of intestinal parasite

Based on microscopic stool sample examinations, eight species of intestinal parasites were identified with an overall prevalence of 33.2%.From the total species of intestinal parasites detected the most prevalent wasprotozoan 109(81.7%) followed by helminths 24(18.3%) (Table 4).

Table 4
Prevalence and type of intestinal parasites among the positive participants in Woreda Medebay Zana towns (February-March, 2019)
Parasites category
Number (%)
Total (%)
Protozoan
 
109(81.7)
 
Entamoeba coli
50(37.4)
 
 
Entamoeba histolytica/dispar
24(18)
 
 
Entamoeba hartmanni
18(13.5)
 
Giardia lamblia
17(12.8)
 
Helminths
24(18.3)
 
Schistosoma mansoni
8(6)
 
 
Hymenolepis nana
7(5.3)
 
 
Enterviousvermicularies
6(4.5)
 
 
Taenia species
3(2.3)
 
Total
133(100%)

Factors associated with the occurrence ofintestinal parasites

The findings from the bivariate analysis showed that 13 variables meet the criteria of p- value < 0.2 to be included for multivariate analysis. From the total of 13 variables that met the criteria only 7 variables were significantly and independently associated with the occurrence of intestinal parasites.

The analysis from the multivariate logistic regression showed that those that use public tap water were11.5 times more likely to be positive for intestinal parasitescompared with those that used private tap [AOR = 11.59, 95% CI = 1.73–77.45], food handlers who washed their hands sometimes before food preparationwere 3.25 times more likely to be positive for intestinal parasitescompared to those who washed always[AOR = 3.25,95% CI = 1.33–7.92]. Those food handlers who washed their hands sometimes by soap and water after visiting toilet were 3.54 times more likely to be positive for intestinal parasites compared to those washedtheir hands always[AOR = 3.54,95% CI = 1.72–7.31]. Similarly, food handlers who have no shower facility in their working area were 3.84 times more likely to be positive for intestinal parasites compared to those who have shower facility [AOR = 3.84, 95% CI = 1.47–10.26]. Food handlers who have habit of eating raw vegetables and meats were 31.9times more likely to be positive for intestinal parasites compared to their counterparts[AOR = 31.92, 95% CI = 10.01–101.80]. (Table 5)

Table 5
Factor associated with occurrence of intestinal parasite from the results of bivariate and multivariate logistic regression among the study participant in Woreda Medebay Zana Towns (February-March, 2019)
Variables
Category
Intestinal parasite
COR(CI)
AOR(CI)
No (%)
Yes (%)
What is the source of water in your working area?
Public tap
Private tap
4(26.7%)
264(68.4%)
11(73.3%)
122(31.6%)
5.95(1.86-19.065)
1
11.59(1.73–77.45)*
1
How often you wash your hands before food preparation?
Sometimes
Usually
Always
8(36.4%)
34(46.6%)
226(73.9%)
14(63.6%)
39(53.4%)
80(26.1%)
5.95(1.91–5.482)
4.95(1.99–12.22)
1
3.25(1.33–7.92)*
4.12(1.13–15.05)*
1
Do you wash your hands by soap and water after visiting toilet?
Sometimes
Usually
Always
6(18.8%)
74(50.3%)
188(84.7%)
26(81.2%)
73(49.7%)
74(15.3%)
5.45(3.34–8.88)
23.96(9.17–62.57)
1
3.54(1.72–7.31)*
6.05(1.67–21.92)*
1
Have you use your sick leave properly to obtain Rx?
No
Yes
56(47.9%)
212(74.6%)
61(52.1%)
72(25.4%)
3.21(2.04–5.03)
1
 
Does your working area have shower facility?
No
Yes
18(34.6%)
250(71.6%)
34(65.4%)
99(28.4%)
4.77(2.57–8.84)
1
3.84(1.47–10.26)*
1
Do you wash your body regularly in your working area?
No
Yes
116(52.4%)
152(84.4%)
105(47.5%)
28(15.6%)
4.91(3.03–7.95)
1
2.48(1.09–5.61)*
1
Do you have habit to eat raw vegetables &meat?
Yes
No
6(12.8%)
264(74%
41(87.2%)
92(26%)
19.46(7.99–47.34)
1
31.92(10.01–101.80)*
1
Does your working area have separate dressing room?
No
Yes
55(48.2%)
213(74.2%)
59(51.8%)
74(25.8%)
3.08(1.96–4.85)
1
 
Do you wear clean aprons when you preparing food?
No
Yes
63(46%)
205(77.7%)
74(54%)
59(22.3%)
4.08(2.61–6.36)
1
 
Variables
Category
Intestinal parasites
COR(CI)
AOR(CI)
No (%)
Yes (%)
Do you wear hair garments during preparing food?
No
Yes
59948.4%)
209(74.9%)
63(51.6%)
70(25.1%)
3.18(2.04–4.98)
1
 
How frequent you cut your fingernails?
(per week)
One times
One times Two times
184(62%)
62(82.7%)
22(75.9%)
113(38%)
13(17.3%)
7(24.1%)
1.93(0.79–4.664)
0.65(0.23–1.864)
1
 
How frequently the kitchen floor cleaned?
(per day)
One times
Two times Three times
35(30.4%)
152(76.4%)
81(93.1%
80(69.6%)
47(23.6%)
6(6.9%)
30.85(12.30-77.38)
4.17(1.71–10.18)
1
13.73(4.21–44.77)*
2.51(0.85–7.39)
1
Monthly income (birr)
500–900 1000–1500
119(56.1%)
149(78.8%)
93(43.9%)
40(21.2%)
2.91(1.87–4.52)
1
 
Note: CI = Confidence interval AOR = Adjusted odds ratio COR = Crude odds ratio * =Significant associated factors

Discussion

In this cross-sectional study, the overall prevalence of intestinal parasites among food handlers was 33.2% in Medebay Zana District, North West Tigray. The prevalence of intestinal parasites in this study was relatively higher than the studies reported in Ethiopia, Aksum Town at 14.5%[14], Gondar, Northwest Ethiopiaat 29.1%[15],North East India at 29.33% [16],Saudi Arabiaat 23%[17],Accra, Ghanaat 21.6%[18], Kenyaat23.7%[19],Omdurman, Sudan at 6.9%[20], Turkeyat 8.8%[21], and Sari and Northern Iranat 15.5%[22]. The prevalence of intestinal parasite in this current study among the food handlers was lower than study done in South West Ethiopia 44.1%[23], Bahr Dar Town 41.1%[24], Jima Town 48.2%[25], Tigray Mekelle Town 49.3%[26], and India Tertiary Care Hospital 40.5%[27].The prevalence of intestinal parasites in the current study wasconsistent with the studiesconducted in Southern, Ethiopia which was 36% [28] and study conducted in Qatar reporting 33.9% prevalence[29].

The variability from our current prevalence may reflect differences in socioeconomic status, climatic conditions, poverty, personal and community hygiene, and period of the study. Differences in the study time might have also contributed as our study was conducted during the time when irrigation movement was high; hence,the entire data set was collected during dry months which may contribute to raising the prevalence of schistosomiasis and other helminths. In many arid or semi-arid habitats, some protozoan parasites are common toward the end of the rainy season [20]. The cultural habit of eating raw meat in some areas may contribute to increasing presence ofhelminths[5].

In the present study, many intestinal parasitic infections were found with S.mansoni being the predominant parasite from helminths followed by Hymenolepis nana. This finding was relatively consistent with a similar study conducted in Aksum Town, Ethiopia[14].E.coliwas the most predominant parasite from protozoan parasites followed by E.histolytica/dispar which resembled findings from a similar study conducted in Southern Ethiopia, reporting the prevalence of (36%) [28].

Poor personal and environmental hygiene, including using public tap water and eating raw vegetables and meat among food handlers is a common practice that contributes to food and water borne as well as skin transmitted diseases[26]. Parasite eggs in the environment can contaminate vegetables and water source, then hands and subsequently foods,hence directly enter into the mouthas can ingested by eating raw vegetables and by scratching skins[22]. Hence, in this study,the untrimmed source of water, washing hands before food preparation, washing hands with soap and water after visiting toilet, shower facilities in the workplace, regular washing of one’s body, habit to eat raw vegetables & meat and kitchen floor cleaned were identified as determinant factors for intestinal parasites among food handlers.

Conclusion

In conclusion, this study revealed a high prevalence of intestinal parasite among food handlers who tested positive for different intestinal parasites.Sourceof water, hand washing after visiting the toilet and before food preparation, shower facilities, washing one’s body regularly, practices related to eating raw vegetables & meat, and kitchen floor cleanedwere the identified factors affecting food handlers risk of acquiring intestinal parasite in the study area.

Declarations

Ethics approval and consent to participate: Ethical clearance was obtained from the Ethical Review Board, Institute of Biomedical Science Mekelle University. The respondents were informed about the objective and purpose of the study and written consent was obtained from each respondent. Confidentiality of the information was assured.

Consent for publication: Not applicable

Availability of data and materials: All data generated or analyzed during this study are included in this published article.

Competing interests: We, the authors, declare no conflict of interests

Funding: This work was not funded by any external funding agent. Mekelle University College of Health Sciences supported the process of data collection.

Authors’ contribution: KR, KT, GB& MT: Conceived and designed the proposal, analyzed the data and wrote the initial version of the manuscript; HG, GG& MT, Wrote the final version of the manuscript. All authors read and approved the final version of the manuscript.

Acknowledgement

We would like to acknowledge the study participants for their willingness to participate in the current study

References

1.           Wegayehu T, T.T., Seifu B, Teklu T.Prevalence of intestinal parasitic infections among highland and lowland dwellers in Gamo area, South Ethiopia. . BMC Public Health. , 2013;  13(1):151.

2.           World Health Organization.Control of leishmaniasis. Report by the secretariat.  2007.

3.           World Health Organization.Soil-transmitted-helminth  Infections. Accessed 28 Apr 2018.

4.           Saboyá MI, C.L., Ault SK, Nicholls RS. , Prevalence and intensity of infection of soil-transmitted helminths in Latin America and the Caribbean countries:Mapping at second administrative level 2000–2010. Pan American Health Organization 2011.

5.           Daryani A, E.G., Sharif M, Ghorbani L, Ziaei H. Prevalence of intestinal parasites in vegetables consumed in Ardabil, Iran. Food Control, 2008;. 19:790-4.

6.           Nyarango RM, A.P., Kadiru EW, Nyanchongi BO.The risk of pathogenic intestinal parasite infections in Kisii Municipality, Kenya. BMC Public Health, 2008; 8:237.

7.           Duc PP, N.-V.H., Hattendorf J, Zinsstag J, Cam PD, Odermatt P. , Risk factors for Entamoeba histolytica infection in an agricultural community in Hanam province, Vietnam. Parasites &Vectors, 2011;. 4(1):102.

8.           Deribe K, M.K., Gebre T, Hailu A, Ali A, Aseffa A, et al.The burden of neglected tropical diseases in Ethiopia, and opportunities for integrated control and elimination. Parasites & Vectors, 2012;. 5(1):240.

9.           Mudey AB, K.N., Mudey GA, Goyal RC, Dawale AK, Wagh VV. Health status and personal hygiene among food handlers working at food establishment around a rural teaching hospital in Wardha District of Maharashtra, India. Global Journal of Health Science. 2010; . 2(2):198.

10.         Arani AS, A.R., Akhlaghi L, Shahi M, Lari AR. Prevalence of intestinal parasites in a population in south of Tehran, Iran. . Rev Inst Med Trop Sao Paulo. , 2008; 50:145-9.

11.         Nigusse D, K.A.Food hygiene practices and prevalence of intestinal parasites among food handlers working in Mekelle university student’s cafeteria, Mekelle. Global Adv Res J Soc Sci (GARJSS). 2012;. 1(4):065-71.

12.         Kidane E, M.S., Kebede A, Desta M. Prevalence of intestinal parasitic infections and their associations with anthropometric measurements of school children in selected primary schools, Wukro Town, Eastern Tigray, Ethiopia. International Journal of Current Microbiology andApploed Sciences,2014; 3(3): 11-29.

13.         Cheesbrough, M., 1998, 2005, 2009.

14.         Gezehegn D, A.M., Tetemke D, Zelealem H, Teklay H, Baraki Z, Medhin G. , Prevalence and factors associated with intestinal parasite among food handlers of food and drinking establishments in Aksum Town Tigray, Ethiopia. 2017,. 17;17(1):819.

15.         Andargie G, K.A., Moges F, Tiruneh M, Huruy K. , Prevalence of bacteria

and intestinal parasites among food-handlers in Gondar town, northwest

Ethiopia. . J Health Popul Nutr. , 2008;. 26(4):451.

16.         Ghosh A, M.P., Sharma VP. , Prevalence of parasitic infestations amongst the food handlers in a city of North Eastern Region of India. . 2014.  source???

 

17.         Zaglool D, O.R., Farooq M., Prevalence of intestinal parasites and bacteria among

food handlers in a tertiary care hospital. Nigerian Medical Journal: Journal of the Nigeria

Medical Association; 2011. 52(4):266.

18.         Ayeh-Kumi P, Q.S., Kwakye-Nuako G, Kretchy J, Osafo-Kantanka A, Mortu S.  , Prevalence of intestinal parasitic infections among food vendors in Accra, Ghana. The Journal of Tropical Medicine and Parasitology. 2009;. 32(1):1-8.

19.         Biwott GK, W.P., Ngeiywa MM., Prevalence of Gastrointestinal Parasitic Infections among Food Handlers in Eldoret Municipality, Kenya. . Journal of Biology, Agriculture and Healthcare. 2014;. 4(27):160-71.

20.         Saeed HA, H.H.Bacteriological and parasitological assessment of food handlers in the Omdurman area of Sudan. Journal of Microbiology, Immunology and Infection. 2010;. 43(1):70-3.

21.         Gunduz T, L.M., Cumen S, Ari A, Etiz S, Tay Z.Prevalence of intestinalparasites and nasal carriage of Staphylococcus areus among food handlersin Manisa Turky. Journal of Environmental Health.  2008;. 18(5):230–5.

22.         Sharif M, D.A., Kia E, Rezaei F, Nasiri M, Nasrolahei M.  Prevalence ofintestinal parasites among food handlers of Sari, Northern Iran. Rev Inst MedTrop Sao Paulo. 2015;. 57(2):139–44.

23.         Tefera T, M.G.Prevalence and Predictors of Intestinal Parasites among Food Handlers in Yebu Town, Southwest Ethiopia. PloS One. , 2014;  9(10):e110621.

24.         Abera B, B.F., Bezabih B. Prevalence of Salmonella typhi and intestinal parasites among food handlers in Bahir Dar Town, Northwest Ethiopia. Ethiopian Journal of Health Development., 2010;. 24(1).

25.         Jejaw A, Z.A., Zemene E, Belay T. Status of intestinal parasitic infections among residents of Jimma Town, Ethiopia. . BMC Research Notes., 2014,. 7:502.

26.         Nigusse D, K.A.Food hygiene practices and prevalence of intestinal parasites among food handlers working in Mekelle university student’s cafeteria, Mekelle. Global Adv Res J Soc Sci (GARJSS). 2012;. 1(4):065-71.

27.         Sande S, B.S., Sande V, Tawade V. Screening of Food Handlers for Intestinal Parasites and Enteropathogenic Bacteria in a Tertiary Care Hospital. International Journal of Health Sciences and Research (IJHSR). 2014; 4(5):88-94.

28.         Mama MA, A.G.Prevalence and factors associated with intestinal parasitic infections among food handlers of Southern Ethiopia. BMC Public Health. (2016) 16:105.

29.         Abu-Madi MA, B.J., Ismail A. Patterns of infection with intestinal parasites in Qatar among food handlers and housemaids from different geographical regions of origin. Acta tropica. 2008;. 106(3):213-20.