Prevalence of Intestinal parasitic infections and associated factors among diarrheal outpatients in South Gondar Zone, Northwest, Ethiopia.

Background : Intestinal parasitic infections are major public health problems in several tropical and sub-tropical developing countries with poor socio-economic status including Ethiopia. Diarrheal patients are a major part of the population with a high risk of intestinal parasitosis. There is a scarcity of studieson intestinal parasite infection among diarrheal patients in South Gondar. As a result, this study was conducted to assess the prevalence and associated factors of intestinal parasite infection among diarrheal patients in this area. Methods : An institutional-based cross-sectional study design was conducted from March to May 2019 with a structured questionnairedata collection technique. A total sample of 240diarrheal patients included in the study and a simple random sampling technique was used. The stool sample from each study subject was collected and analyzed by direct wet mount techniques. Data were entered in Epi Data Version 4.6.0.0 and exported to Stata version 14 for analysis. Binary logistic regression was used to measure the association of factors with the outcome variable. Factors that have an association with the outcome variable at p-value 0.25 was taken into the multivariable logistic regression analysis to control the potential confounders. The result of the final model will be expressed in terms of adjusted Odd Ratios (AOR) and 95% confidence interval (CI) and statistical significance will be declared if the P-value is less than 0.05.


Introduction
Intestinal parasitic infections affected more than 3.5 billion people globally and leads to clinical morbidity for around 450 million individuals (1,2).
Intestinal Parasites (IP) are organisms that infect the gastrointestinal tract of humans and other animals. Helminths and protozoans are the main types of intestinal parasites. Helminths are worms with many cells, which can be divided into Nematodes (roundworms), Cestodes (tapeworms), and trematodes (flukes) while protozoan parasites are parasites that possess only one cell and can multiply inside the human body (3).
From intestinal parasitic infections; Entamoeba histolytica, Giardia lamblia, Ascaris lumbricoides (roundworm), Trichuris trichiura (whipworm), and Necator American's (hookworm) are considered to be a global public health concern and the major public health significant parasitic infections. These intestinal parasitic infections have been recognized as significant causes of illnesses and diseases worldwide (4)(5)(6).
Intestinal parasitic infections are frequently reported in the poor communities of developing countries and within these, the majority of the cases occur among diarrheal patients (7). Diarrheal diseases are the major causes of morbidity and mortality in the developing world (8). Intestinal parasitosis is more prevalent among diarrheal patients as compared with the general population. About 12% of the global disease burdens caused by intestinal parasites are observed among diarrheal patients in developing countries (9).
Intestinal parasitic infections are usually highly prevalent among the resource-poor and socioeconomically deprived communities where overcrowding, poor environmental sanitation, low level of education, and lack of access to safe water are prevalent (10). The infected people experience a vicious cycle of undernutrition and repeated infections leading to excess morbidity with children being the worst affected (9).
Health promotion and education aimed at improving personal hygiene, and community-based mass deworming are currently practiced prevention and control strategies targeted to void transmission of IP (11). However, the burden and consequence of intestinal parasitic infections are still increasing in poor communities. Regarding Giardiasis, it is the most predominant protozoan infection that affects approximately 200 million people in the world and 20 to 30 % of developing countries. Amoebiasis due to infections with the intestinal protozoon Entamoeba histolytica results in 40,000-100,000 deaths each year (12,13).
Scholars claimed that environmental, social, and geographical factors such as low household income, poor personal and environmental sanitation, overcrowding, limited access to clean water, tropical climate, and low altitude significantly associated with the occurrence of high intestinal parasitic infections especially in tropical and sub-tropical areas (14,15).
In Africa, more specifically Sub-Saharan Africa including Ethiopia, parasitic infections are highly abundant (16). For instance, recent estimates indicated that approximately 1472, 1298 and 1049 million people have roundworm, hookworm, and whipworm infection, respectively (17).
In Ethiopia, intestinal parasitic infection is one of the top ten causes of morbidity amongst children (18,19). Parasitic helminths are the second most predominant causes of outpatient morbidity in the country andNorthwestern Ethiopia is highly affected as compared to other parts of Ethiopia. (20,21).
Intestinal parasites particularly intestinal protozoa parasites are the major cause of diarrhea and are easily transmitted from one individual to the other through different routes including eating unwashed vegetables, contaminated food, and water. On the other way, diarrheal patients are reported to be at high risk for severe infections and mortality associated with intestinal parasitic disease (22).There is no published data in the study area that shows the prevalence of intestinal parasites among diarrheal patients and possible predictors. Therefore, the main purpose of this study was to assess the prevalence of intestinal parasites among diarrheal patients and associated risk factors.

Study Area
The study was conducted onNefas Mewecha Health Center (NMHC), South Gondar zone, Am-

Data Collection technique
Socio-demographic characteristics and other associated factors (personal hygiene, age, sex, source of water) data were collected through face to face interview by using a pre-tested structured questionnaire. The study subject was asked to provide at least 3grams of stool. Each stool sample was examined by using the wet mount and formal-ether concentration. The wet mount method was performed on a 0.5-gram stool and for the formal-ether concentration,the method was used 2 grams of stool the ova, cyst, and larvae of different intestinal parasites separately reported.

Data Quality control
Data quality was ensured at various activities of the study by the following standard operating procedure (SOP). The questionnaire was translated to the Amharic language by the principal investigator and at the end translated back to English. After the data collection process, the data were checked for completeness. Before starting the actual work, the quality of the reagent and instruments were checked for the expiry date. The specimen was also being checked for the serial number, amount, consistency, quality, and procedures of collection. Positive quality control and negative quality control slides, as well as a colored atlas, were used as a guideline. Then the result of the laboratory examination was recorded in a well-prepared format carefully and finally attached with the questionnaire accordingly to their codes.

Data processing and Analysis
Data were entered in Epi Data version 4.6.0.0 and exported to STATA software version 14 for data cleaning and analysis (20). Descriptive statistics like frequency and percentage was calculated to describe the study population characteristics. The strength of associations will be measured by binary logistic regression at a 95% confidence interval and a p-value of 0.05 was being used as a cut of a point. Variables with a p-value of less than 0.2 were incorporated into multivariable logistic regression. Results were reported as AOR (adjusted odds ratio) with 95% CI.

Socio-demographic characteristics among diarrhea patients
A total of 240diarrheal patients were included forthe final investigation. However, 4(1.6%) were excluded because of the inability to provide specimens. Among the study participants,131 5 (54.6%) patients were female. Nearly halves (48.7%) of the study participants were from a rural place of residence and 84 (35.0%) had no formal education i.e. unable to read or write. A higher proportion of respondents were married (50.4%), Orthodox Christian (83.8%), and Farmer (44.6%)(Table1). Hygiene and Sanitation related characteristics 6 Almost all (90.0%) of the study participants came from a household that had a latrine facility. Of the total participants, about 45.4% had a habit of handwashing after the toilet and 86.6% had a habit of wearing shoes. Moreover, halves (52.9%) of the study participants used tap water sources.Most (80%) of the study participants had practicing fingernail trimming (Table 2).

Prevalence of intestinal parasites and distribution of parasites
The overall prevalence of single or multiple intestinal parasitic infections among diarrheal patients was45.4% with a 95% CI of 39.2% to 51.8%. Different types of parasites were detected from the stool samples of study participants. Prevalence of Entamoeba histolytica/dispar (E. histolytica/dispar) was the highest 60(55.5%) and followed by Giardia lamblia (G. lamblia)

Factors associated with intestinal parasites among diarrheal patients
Sex, age, religion, marital status, a habit of handwashing after toilet, a habit of purifying water before drinking, shoe-wearing habit, and cleanliness of finger was incorporated into multivariable logistic regressionsince P-value less than 0.25. According to multiple logistic regressionshoewearing habit,marital status, and cleanliness of fingerswere statistically significant associated factorsto intestinal parasitic infections ( Table 3).   (20,21,24).
However, it was lower as compared to findings in Yemen and studies in the Amhara region;Motta health centers,and districts in Bahirdar (25,29).
In this study, the most prevalent parasitic infection was Entamoebahistolytica(55.5%) followed by Giardia lamblia (24.1%). Ascaris lumbricoid,Hookworm, and Enterobius vermicularis was the least in prevalence.The pattern and distribution of IPs were similar to astudy conducted in Yemen, Arba Minch (25,26).
Those patients who had no clean fingernailshad 5.12 times higherodds to havean intestinal parasitic infection as compared to those who had clean fingernails.Similar to this finding, a study conducted in different setups showed that fingernail status is significantly associated with intestinal parasitic infection (20,25,26).The association could be justified as the leading IPs in this study Enteameoba histolytica and Giardia lamblia primarily transmittedfecal-orally.Unclean fingernails havethe main roleinthe fecal-oral transmission of intestinal parasites through not washed or unclean hands.
The odds of intestinal parasitic infections were 2.81 times higher among the diarrheal patients who had no shoe wearing habit as compared to those who wear shoes frequently.Similar to this study conducted in Debreelias and Bahir Dar showed that patients who had no habit of wearing shoes were more infected with intestinal parasites than havinga habit of wearing shoes (19,29).This could be explained through; 3.7% of diarrheal patients who visited the targeted health centers were infected with hookworm parasites. Being barefooted or not wearing shoes is the main route of exposure for hookworm. This finding implies that some parts of the community practiced shoe-wearing less frequently and a proportion of them was infected with hookworm and other pathogens.
Age, sex, a habit of handwashing after toilet, and usage of purified water were not statistically associated with the occurrence of intestinal parasitic infections in this study.

Conclusion
Intestinal parasitic infections were a highly prevalent health problem among populations in Lay Gaynteworeda. The risk factor of the prevalence of intestinal parasites was poor hygiene of fingernails and no shoes wearing a habit.All these factors including shoe-wearing habits and keeping fingernails clean play an important role in preventing patients from infection with intestinal parasites. The habit of wearing shoes was found to be a protective factor for hookworm infec- Nefas Mewcha Health Center.

Ethical Consideration
The study was approved by Debre Tabor University, college of health science ethical review committee. Permission was obtained fromthe administrator and workers of NMHC. The health center authorities, professionals, and the patients were informed about the purpose and procedures of the study. Informed consent from each adult respondent and informed assent from legal guardians or parents of children were obtained.Confidentiality was observed and an unauthorized person is not access to the data collected. Each subject was assigned a study identification number, and these subject identifiers will notbe released outside the researcher. Data is only accessed by the authorized person. The methods and procedures were conducted according to Debretabor university regulations and guidelines.

Not applicable
Availability of data and materialsThe data sets in this study are available from the corresponding author on reasonable request Competing interestsThe authors declare no competing interests