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Intestinal Parasitic Infections Among Patients Who Visited Woldia Comprehensive Specialized Hospital’s Emergency Department Over a Six-Year Period, Woldia, Ethiopia: A Retrospective Study

Background Despite ongoing intensive public health intervention efforts, intestinal parasitic infections (IPIs) remain a major public health problem in developing countries, including Ethiopia. Having updated epidemiological data focusing on the top common IPIs that cause emergency visits is crucial for implementing area-specific and evidence-based intervention strategies. Hence, this study aimed to determine the prevalence of IPIs in Woldia Comprehensive Specialized Hospital’s (WCSH) emergency laboratory over a six-year period. Methods An institutional-based retrospective study was conducted to assess the prevalence of IPIs over a six-year period (2014–2019) using a recorded saline wet-mount stool sample examination result in the laboratory logbook at WCSH’s emergency department. Results In this study, of the total of 11,281 clinically suspected individuals who were requested for stool sample examination, 3908 (34.6%) individuals were diagnosed with IPs. The majority of confirmed cases were caused by protozoan parasites (32.9%), followed by helminth infections (1.7%). A slight fluctuating trend in the prevalence of IPs was observed in the six-year study period, with the highest prevalence documented in the year of 2014 (41.3%) and the lowest in 2017 (28.0%). Entamoeba histolytica/dispar and Giardia lamblia accounts for 95% of the IPs. The prevalence of protozoan infection was significantly higher in females (p-value = 0.0101), while H. nana (p-value =0.0138) and E. vermicularis (p-value = 0.0201) infections were higher in males. The highest and the lowest IP prevalence were reported in the age groups of 45–54 years (40%) and under five years (25.6%), respectively. Conclusion and Recommendations In the study area, nearly one-third of patients with emergency visits due to gastrointestinal symptoms were infected with IPs. This underlines the severity of the problem in the study area, which requires a collaborative effort of concerned bodies to minimize the burden of IP to the level where it is no longer a public health threat.


Introduction
Although intestinal parasitic infections (IPIs) are preventable neglected tropical infections, they continue to be a major public health issue that blights the lives of billions of people worldwide. 1 The public health consequences of IPIs are particularly pronounced in the tropical and subtropical regions of low-income countries where potable water is scarce, sanitation is poor, and people are experiencing substandard lifestyles. 2 Soil-transmitted helminths like Ascaris lumbricoides (A. lumbricoides), Trichiuris trichiuria (T. trichiuria), and hookworms are among the most prevalent helminth infections whereas Entamoeba histolytica (E. histolytica) and Giardia lamblia (G. lamblia) are the predominant protozoan infection. 3,4 In particular, protozoan parasites account the majority causes of IPIs than helminths in developing countries. 3 Globally, an estimated 3.5 billion people are affected; 450 million are symptomatic, and more than 200,000 people deaths are reported annually due to IPIs. 5,6 Infections with IPs are not only responsible for morbidity and mortality but they also cause nutritional problems (such as stunted growth, low vitamin A, iron deficiency anemia, weight loss, and chronic blood loss), as well as compromise psychological and social wellbeing. Mental development impairment also the other public health challenges of IPIs, particularly in children (such as impaired growth, decreased school attendance, cognitive impairment, decreased educational achievement, and adult productivity). 1,6 In particular, Sub-Saharan Africa (SSA) countries disproportionately take the lion share of the global burden of the IPIs in association with poor socio-economic status, lack of pure water supply, poor sanitation, inadequacy of healthcare center, poor community awareness as well as the prevailing bad climatic and environmental conditions. 4,7,8 Existing evidence indicates that the prevalence of IPIs in different areas of SSA exceeds 50%. 9 Among SSA countries, Ethiopia ranks second only to Nigeria in the prevalence of IPIs, accounting for approximately 50,000 deaths annually in the country. 1,10 However, the World Health Organization (WHO) continues to face challenges in achieving its goal of eliminating or reducing IPs, many of which are Neglected Tropical Diseases (NTDs), to the point where they no longer pose a public health threat in endemic areas due to a lack of updated epidemiological data on the burden of IPs and delivering alternative intervention packages. 11 Thus, conducting longitudinal studies in different localities are crucial in designing and implementing effective preventive and control strategies for IPs in Ethiopia, where there is a significant economic constraint on medicine purchase and mass treatment. Furthermore, identifying the common parasitic infections that cause people to visit emergency healthcare facilities in a particular community is critical for developing area-specific, evidence-based public health intervention programs. Despite this, compiled epidemiological findings on the magnitude of IPIs in the study area and surrounding community have not previously been disseminated in the scientific community, and the current study is the first to our knowledge. However, although the burden of parasitic infections in the study area has not previously been well documented in scientific journals, health professionals working in the area report that a significant number of individuals visiting the emergency department are due to parasitic infection. Therefore, this study was designed to determine how many clinical cases in the community that require immediate medical care are due to IPI and to prioritize the top IP species among patients who visited WCSH's emergency department between 2014 and 2019.

Study Area
This study was conducted in WCSH's emergency department in Woldia town, Northeastern Ethiopia. Woldia serves as the administrative center of the North Wollo zone of Amhara regional state. The town is located at a latitude of 11°46′ 50 "N and a longitude of 39°36′ 0"E with an elevation of 2112 meters above sea level. According to the 2014 national population project conducted by the central statistical agency of Ethiopia (CSA), there are about 180,000 inhabitants in the town. Regarding the health infrastructure, the town has one public hospital, two public health centers, and more than fifteen private clinics. The hospital has been serving the residents of North Wollo as well as nearby populations from the Tigray and Afar regions.

Study Design and Population
A hospital-based retrospective study was conducted to determine the prevalence and distribution of IPIs over the last six years at the emergency department of WCSH. All individuals suspected of having an IPI who provided stool samples for examination using the direct wet mount laboratory method and were registered in the hospital's emergency laboratory logbook were included in the study population.

Inclusion and Exclusion Criteria
Participants who had full recorded data such as age, sex, and year of diagnosis were included in the study, whereas individuals who had incomplete recorded information in the logbook were excluded.

Data Collection Tools and Techniques
Prior to extracting our variable of interest for this study, a data extraction sheet that was specifically designed to extract participants' demographic data (age, gender), year of diagnosis, and laboratory investigation results was prepared using Microsoft Excel. Then, clients' gender, age, date of diagnosis, and species of parasite detected were transferred from the laboratory logbook to the preprepared data extraction excel sheet. Only data from individuals with a complete record of data in the laboratory logbook were collected. Based on this, we extracted data for only 11, 281 clinically suspected individuals for intestinal parasitic infections who had stool examinations between 2014 and 2019. All extracted stool examination results were examined using the direct saline wet-mount laboratory technique, which is the only laboratory method used in the hospital laboratory for the diagnosis of intestinal parasites. To assure the quality and consistency of the data, data collectors were trained regarding the data extraction tool, variables of interest, and the objective of the study. Besides, every activity of the data extraction and entry process was supervised by the study team members.

Data Processing and Analysis
Data were coded and checked for completeness using Epi-data software before being transferred to SPSS software for statistical analysis. Descriptive statistics were used to show the distribution of IP in terms of individuals' sex, age, and diagnosis year. A Pearson's X 2 test was used to assess the association between variables, and a p-value of < 0.05 was considered statistically significant. The results were displayed using text, graphs, and tables.

Result
Over the six-year period, a total of 11,281 patients were requested stool sample for the diagnosis of IPs at the Woldia hospital emergency laboratory. Of these, the majority, 5968 (52.9%), were females. The age of the patients ranged from 1 to 95 years, with a mean age of 24.68 (±16.62 SD) years. The highest proportion of patients visiting the hospital emergency laboratory unit for IP examinations was within the age group of 15-24 years (28.5%), followed by 25-34 (21.8%) and 5-14 (14.6%) years. Overall, infection with intestinal parasite was found to be 34.6% (3908/11,281) with a fluctuated trend prevalence across years ranged from 28.0% to 41.3%. The highest prevalence of intestinal infections was recorded in the year of 2014 (41.3%) while the least case in 2017 (28.0%) (Figure 1). The IP infection rate was found to be higher in patients with an age group of 45-54 years (40%), followed by >54 years (39.2%) and 25-34 (37%) years ( Table 1).

The Proportion of IPs
Overall, eight IP species were detected in this study. Of these, two were protozoan parasites, which were responsible for the majority of the case in the study area, 3716 (95%). Entamoeba histolytica/dispar 2306 (59%) was the leading IP responsible for emergency admission, followed by G. lamblia 1174 (30%), and mixed infection (Entamoeba histolytica/ dispar and G. lamblia) 236 (6%). While helminthic infections account the least case among individuals who visited emergency unit for immediate medical care with the predominant species of Ascaris lumbricoides (1.9%) (Figure 2).

The Gender Based Prevalence and Distribution of IPs
The rate of IPIs was significantly higher in females than males (P-value = 0.0277). The overall prevalence of protozoan infections was significantly higher in females (34%) than males (31.7%) (P-value = 0.0101). The rate of E. histolytica/ dispar infection in female patients was higher than their counterparts (P-value = 0.0163). However, H. nana (P-value = 0.0138) and E. vermicularis (P-value = 0.0201) infection rates were higher in male patients ( Table 2).

The Distribution of IPs in Different Age Groups
The overall IP positivity rate was slightly increased as the age of the patient increased. Furthermore, an increased protozoan infection rate with age was seen. The highest intestinal protozoan infection rate was observed in patients aged 55 years and above, followed by the 45-54 age groups and the 25-34 age groups. However, the highest helminth infection rate was observed in patients aged between 5 and 14 years, followed by the 45-54 age group and the 15-24 age

Discussion
Protozoa and helminths are among the etiologies of diarrheal diseases, and infections due to these pathogens are the major public health problems worldwide, especially in the developing world where poverty, lack of drinking water, lack of health education, or lack of sanitation facilities are prevalent. 7,8,12 In the present study, we performed a six-year retrospective analysis of IP at the emergency laboratory of WCSH, Woldia, Northwest Ethiopia. The results showed that IPs are one of the major reasons for emergency admission. About 34.6% (95% CI = 33.8-35.5%) of patients admitted to WCSH's emergency department were infected with at least one IP. This figure indicates that nearly one-third of emergency admissions among emergency admitted patients with gastrointestinal symptoms are due to IPs.

Frequency of parasite
The frequency and percentage of IPs     availability of quality water supply in the study area, sanitary or hygiene practices, socioeconomic status, the study period, geographic areas, and the methods employed for stool examination could affect the IP prevalence rate.
In the present study, eight different types of IPs were detected among individuals who had a stool sample examination in the emergency laboratory. The protozoan parasites, E. histolytica/dispar and G. lamblia, accounted for 95% of the parasites, and the remaining 5% were helminths. E. histolytica/dispar was the leading parasite, which accounted for about 65%, followed by G. lamblia, which accounted for 30%, and Ascaris lunmbricoides (1.9%). Although a huge variation in numbers was seen, regarding the predominant parasites, similar findings were also reported in other parts of Ethiopia. 13,15,17,27 The higher prevalence of intestinal protozoa infections in this and other studies might be due to the presence of inadequate water supply, sanitation activities, food safety, and hygiene behaviors in the population. [31][32][33][34] Lack of safe drinking water and sanitation facilities such as toilets is highly associated with a high risk of intestinal E. histolytica/dispar 35 and G. lamblia 36 infections. Furthermore, the very high proportions of intestinal protozoa infections in this study might also be associated with the population that participated in the study; all the data was taken from emergency patients. Protozoan parasites such as E. histolytica can cause severe watery or bloody diarrhea with reduced appetite and weakness and lead to hospital emergency visits. 37,38 The lower prevalence of intestinal helminth infections in most of the Ethiopian studies could be due to a deworming program, particularly for soiltransmitted helminths, initiated long ago in Ethiopia. 39 The overall prevalence of protozoan infections (32.9%) was higher than helminth infections (1.7%). Similar to the present study, reports from other parts of Ethiopia showed that protozoan infections were more prevalent than helminth infections. 15,27,28 The rates of overall IP infection and protozoan infection were significantly higher in females (35.57% and 34%) than in males (33.6% and 31.7%), P-values = 0.0277 and 0.010, respectively. Despite the lack of compelling scientific reasons, this disparity could be explained by the fact that this study was limited to the emergency diagnosis center, as well as the highest burden of E. histolytica, which accounts for the majority of the estimated prevalence of IPIs in the study area. The main reason why we relate this disparity with the highest cases of E. histolytica and the study center is that existing evidence suggests that males are more asymptomatic carriers of E. histolytica than females. 40 Because of this, females are more likely than males to visit an emergency treatment center to receive immediate medical care. Surprisingly, this finding is not supported by other previously published research works, 16,20,27,29,41 where males were more affected than females. Other few reports also revealed that there was no association between gender and IPIs. 42,43 Regarding the distribution of IPs among age groups, it was higher in the age groups of 45-54 years (40%), > 54 years (39.2%), and 25-34 years (37%). However, it was lower in age groups < 5 years (25.6%), 15-24 years (33.6%), and 5-14 years (34.7%). The prevalence of IPIs among <15, 15-35, and > 35 years was 30.6%, 35.3%, and 39.6%, respectively. In the current study, the age-specific prevalence trend of protozoan parasite infections was increased with age. However, a fluctuating age-specific prevalence trend of helminth infections was found. The higher proportion of PIs in the older population may be attributable to a variety of factors, including agricultural practices and, thereby, migration for labor work, which force them to drink contaminated water and may leave them unable to exercise proper personal and environmental hygiene.
In this study, we have seen a fluctuating prevalence rate of IP infection throughout the diagnosis years. The rate of infection ranged from 28.0% in 2017 to 41.3% in 2014. The infection burden decreased slightly over four consecutive years (2014-2017) but began to rise again in the last two years (2018-2019). Similarly, this fluctuating trend prevalence of IPIs was also supported by other previously conducted research works. 16,26,27 The activities towards prevention and control of infections, education, as well as the quality of life of the population in different years, related to the socioeconomic status of the population, could explain the likely trend variation.

Limitation
This was a retrospective study that did not identify important factors such as water source, sanitary and hygiene habits, latrine availability, the presence of other comorbidities, and whether the patients had been dewormed. Moreover, only wet mount microscopy was employed for the diagnosis, which could underdiagnose parasitic infections in cases of light parasitic load.

Conclusion and Recommendation
The rate of IPI in the WCSH's emergency setting is high. Protozoan parasites E. histolytica and G. lamblia were the most common causes of emergency hospital visits, underlining the need for a safe water supply and food preparation to reduce their burden. The high infection rate calls for a joint effort of healthcare workers and managers as well as other stakeholders for the provision of health education, effective health policy implementation, and public mobilization. Further studies which focus on the risk factors of IPIs in the study area while employing more sensitive laboratory methods should be encouraged.

Data Sharing Statement
All data generated or analyzed during this study were included in this article. Data that support the findings of this study are also available from the corresponding author upon reasonable request.

Ethical Approval and Consent to Participate
Before the commencement of the study, we obtained ethical clearance from Institutional Review Board of Woldia University, and an official letter of cooperations was provided to WCSH. Before data collection, we explained the study objectives to the heads of the hospital and laboratory unit. Since we used secondary data for this study, we didn't require the patient's informed consent. We conducted the study following the Declaration of Helsinki. 44 To maintain the confidentiality of information from participant's record, we didn't record any personal identifiers on the data collection sheet rather we used specific identification code for each recorded participant data, and secured data from participant records were not available to anyone except for the investigators.