Prevalence of intestinal parasites in Erbil, Iraq

Intestinal parasitic infections are caused by intestinal protozoan parasites and helminths, which are widely distributed throughout the world. Infections with intestinal parasites are the most common infections (Haque, 2007) and considered as the significant health problem in developing countries (Jejaw et al., 2014). The diseases burden associated with parasitic infections of the digestive system is massive. Globally about two billion people are affected, with 300 million suffering from severe morbidity (Östan et al., 2007). These infections with intestinal parasites are associated with overcrowding, poor sanitation and malnutrition, contaminated food and water, and poverty (Chala, 2013). Intestinal parasites infect people of all ages, but small children and pregnant women are highly susceptible (Jejaw et al., 2014).

Protozoan and helminthic infections may cause serious public health problems which may include: malabsorption, abdominal pain, hemorrhage, diarrhea, reduced work ability and negative impact on growth, especially in children (Pino Santos et al., 2014). The prevalence of different intestinal parasite species varies from country to country and even from region to region within a country. The objective of this study was to determine the prevalence of intestinal parasites in people living in Erbil province in Iraq between 2011 and 2021, and their association with some epidemiologic risk factors such as age, gender, month, and year. This retrospective cross-sectional study is the first in the province of Erbil which include the data of 11 years. Public health service can use these prevalence data to better understand the epidemiology of intestinal parasites in the province, develop strategic policies to prevent the spread of infections, and establish research priorities.

The current study was reviewed and approved by the Scientific Committee of the Biology Department in Salahaddin University— Erbil. It was conducted in accordance with the Declaration of Helsinki. An official letter was written to the directorate of preventive health affairs in Erbil for permission. No patient names were collected from the data.

The overall prevalence of intestinal parasites among tested patients was 26034 (4.24 %) out of 614455 included individuals. There was an increase in the number of collected stool samples since 2011 until 2015 and then it was followed by a linear decrease until 2018, the number of samples increased again in 2019. The proportion of patients positive for intestinal parasites decreased from 16.72 % in 2011 to 6.64 % in 2018, then increased to 8.60 % and 7.74 % in 2019 and 2021 respectively (Fig. 1). The maximum number of laboratory diagnosed cases of intestinal parasites was reported in 2011 with 4352 infected persons and the minimum was reported in 2020 with only 167 infected persons.

Fig. 1

Positive cases for intestinal parasites by year in Erbil province, Iraq.

Source: data from directorate of preventive health affairs in Erbil province, Iraq.

In this study, nine different species of intestinal parasites were identified in the laboratory registries of the stool specimens of the patients, two protozoans (Entamoeba histolytica/dispar, Giardia lamblia), and seven helminth species (Enterobius vermicularis, Hymenolepis nana, Taenia Saginata, Ascaris lumbricoides, Trichuris trichiura, Ancylostoma duodenale and Strongyloides stercoralis). The prevalence of protozoan infection was nine times the prevalence of helminthic infection. The prevalence of intestinal protozoa and helminths were 90.47 % (23552/26034) and 9.53 % (2482/26034), respectively.

Only two protozoan parasites had been recorded by the facilities of health care centers in Erbil province, E. histolytica/dispar and G. lamblia. The highest prevalence was due to E. histolytica/dispar (60.92 %) and followed by G. lamblia (29.54 %). The highest and lowest numbers of infected persons with E. histolytica/dispar (2181 and 132) were recorded in 2011 and 2020 respectively. The same years also recorded the highest and lowest numbers of infected persons with G. lamblia (1509 and 27) in 2011 and 2020 respectively. The numbers of infection with protozoan parasites declined in 2018, then the number of cases showed an escalation in 2019 (Table 1).

Intestinal helminthic infections were identified as E. vermicularis (8.56 %), H. nana (0.68 %), T. saginata (0.16 %), A. lumbricoides (0.08 %), T. trichiura (0.04 %), A. duodenale (0.01 %) and S. stercoralis (0.004 %) as shown in Figure 2. Helminthes (A. duodenale, T. trichiura, H. nana and T. saginata) were higher in 2012, while E. vermicularis and A. lumbricoides were higher in 2011 and 2019 respectively. The prevalence of E. vermicularis and H. nana declined over the years, which dropped to only 29 and 7 respectively in 2021. By 2015, till 2021, no cases of A. duodenale, T. trichiura and S. stercoralis were diagnosed. In 2016 – 2021, Erbil reported no cases of T. saginata for the first time, and there were no cases of A. lumbricoides after 2020 (Table 1).

Fig. 2

Intestinal parasites from 2011 – 2021 in Erbil province, Iraq.

Source: data from directorate of preventive health affairs in Erbil province, Iraq.

Furthermore, males had higher overall prevalence rate of infection (65.73 %) compared to Females (34.27 %).

Analyzing the age trends of infection revealed that patients of age group ranging from 15 to 44 years old had the highest prevalence rate at 52.32 % when compared to other age groups, and the lowest (2.78 %) was in infants less than one year of age. The highest prevalence of protozoan infection was found in the 15 to 44 aged group (55.56 %), while prevalence of helminthic infection was higher in the younger age group of 5 – 14 years (48.59 %). One age group was responsible for all the infections with A. duodenale which included children and adolescents aged 5 – 14 years (Table 2).

In terms of seasonality, monthly prevalence of infections increased to the maximum of 2431 and 2485 in January and February, respectively, while the lowest prevalence was registered in March and December (1715 and 1901 respectively) as shown in Figure 3. Monthly accumulated infections with A. duodenale, H. nana and T. saginata presented the highest peak (18.24 %, 9.54 % and 9.76 % respectively) during February. S. stercoralis, E. vermicularis and G. lamblia were more frequently detected in January (9.79 %, 9.54 % and 9.31 % respectively). The number of patients infected with T. trichiura and E. histolytica/dispar peaked in April 37.84 % and 31.82 % respectively, while A. lumbricoides was especially frequent in November (10.45 %), as shown in Table 3.

Fig. 3

Cumulative monthly distribution of intestinal parasites cases in Erbil province, Iraq.

Source: data from directorate of preventive health affairs in Erbil province, Iraq.

Statistically significant relations (p <0.05) were found between the incidence of parasites and each of the sex and age of the patients, year and month.

As per our knowledge, this is the first retrospective cross-sectional study in Erbil province analyzing the results of 11 years of intestinal parasitic infections. Infection with Intestinal parasites considered as neglected tropical disease and is a global public health problem (Jejaw et al., 2014). Planning and evaluating the current in order to design an appropriate intervention program need maintaining frequent monitoring and tracking the trend distribution of intestinal parasite infections in each community. Accordingly, the current study made an effort to analyze and assess the prevalence of intestinal parasites in the province of Erbil between 2011 and 2021.

In the current study of data records, the overall prevalence of intestinal parasitism over the last eleven years was 4.24 % in Erbil province in Iraq. This result was lower than those found in other studies in Iraq. In previous studies conducted in the country, prevalence rates of parasitic infections in hospital patients varied from 7.36 % to 84.67 % and 0 % to 18.01 % of the protozoa and helminth infections respectively (Mahdi, 2022). Although our findings were in agreement with studies reported in Istanbul, Turkey (4 %), the prevalence of intestinal parasitic infections contrasts strongly with that reported in northern Jordan, Van province in Turkey and southern district in Tehran, Iran (44 %, 34.1 % and 10.7 % respectively).

From 2011 to 2015, intestinal parasitic infection rates appear to be decreasing. Possible reasons for the decreased rates of infection during this period might include increasing living standards and hygienic practices in Erbil province, which is part of the Kurdistan region in Iraq, because of the economic boom during this period in the region as a result of high crude oil prices in an oil-dependent country's economy with oil prices recorded more than 100 U.S. dollars per barrel. After that, the economic crisis hit the region, leading to reduced GDP growth and increased poverty. Low-income and poverty are considered as an important risk factor for infection with intestinal parasites. Several studies have shown higher prevalence as a result of lower socioeconomic conditions (Östan et al., 2007; Mehraj et al., 2008; Singer et al., 2020).

For the first time in 11 years, the prevalence of intestinal parasites in Erbil province showed a great decline in 2020. This decline could be related to the absence of data during the quarantine due to the COVID–19 pandemic. People in lockdown also may face difficulties getting public health help to diagnose intestinal parasites. Also, the quarantine period increased people's sensitivity to personal hygiene measures, leading to lower infection rates. These reasons resulted in a decrease in the prevalence of intestinal parasites in 2020.

The results of this study showed the incident of nine intestinal parasites of public health importance among residents of the province. The rate of intestinal parasites varies by age and sex. The 15 – 44 years age group harbored more than the half of the intestinal parasitic infections (52.32 %), followed by those aged 5 – 14 years, while infants >1 year (2.78 %) were the least infected age group. This can be explained by the characteristics of the young and active age group (15 – 44 years), such as eating in restaurants and the difficulties in ensuring hygiene in all restaurants. Infants smaller than one year old recorded the lowest rate of intestinal parasitic infection. This may be due to the fact that during the first six months of life, infants should be exclusively fed on human milk, so there is little chance of eating contaminated raw vegetables and fruits.

The finding of present study is consistent with a previous study carried out in Debre Tabor, Northwest Ethiopia from 2017 to 2021 (Workineh et al., 2022), where the highest intestinal parasitic infections were recorded in the age groups of over 14 years (27.7 %). A 6-year retrospective study of patients attending two hospitals in French Guiana reported the prevalence of intestinal parasites to be 67.7 % among the 18 – 64 year old group, but they recorded 3.3 % in patients less than one year old, which is higher than the finding of our study (Aboikoni et al., 2021). Our findings are in agreement with previous studies in Sharjah, in the United Arab Emirates, where the highest rate of infection with intestinal parasites was reported in the age groups 26 – 34 years (Dafalla et al., 2017).

Regarding protozoan infection, the age group 15 – 44 years showed the highest association of infection than other age groups. The burden of these protozoan parasites in developing countries is mainly due to fecal contamination as a result of poor sewage and poor water quality. In Iraq, the fresh and tap water could be contaminated with pathogenic protozoan parasites like E. histolytica/dispar and G. lamblia in some provinces (Todd, 2023).

Prevalence of helminthic infection was higher in the age group 5 – 14 years. The possible reasons might be due to children playing with soil which facilitates the infection with the helminthic parasites including soil–transmitted helminths.

The prevalence of intestinal parasitic infections is higher in males than females in most age groups, especially among adults aged 15 – 44 years, which was 3.45 times higher than in females for this age group. this could be explained by the immunological differences exist between the sexes that may contribute to increased parasitic infection in males compared to females (Klein, 2004). The other reason may be due to fact that these males recorded higher outdoor activities than females in the province, which increases their susceptibility to parasitic infections. The finding of the present study was similar to the findings of previous studies performed across Iraq which reported higher rates of infection in males than females (Mahdi, 2022). These findings that males are more likely to be infected are also found in other countries, such as in N'Djamena in Chad Republic where males recorded higher infection rates with intestinal parasites (Hamit et al., 2008). Infection with intestinal parasites in expatriate workers in Sharjah in United Arab Emirates were associated with gender as males showed higher infection rates than females (Dafalla et al., 2017). Also, students attending clinic at university of Gondar in Ethiopia showed higher infection rates in males than females (Derso et al., 2021).

The protozoan infection rate was 9.58 times greater than that of helminthic infection. Other studies also reported higher infection with protozoa than helminths in Riyadh, the capital of Saudi Arabia and in Sana'a, the capital of Yemen (Abdelkareem et al., 2022; Al-Yousofiet al., 2022). This may be due to the method of transmission and life cycle of the protozoan parasites which facilitate human infection with them more than helminthic parasites. This finding contrasts with that reported in rural and remote west Malaysia where infections with soil-transmitted helminth were higher than infections with protozoa (Ngui et al., 2011).

Only two species of protozoan parasites (E. histolytica/dispar and G. lamblia) were detected in the feces of patients in Erbil province. This could be due to the use of only wet mount method for diagnosis in health facilities in the province.

E. histolytica/dispar was the most prevalent intestinal parasite with a rate of 60.92 % in our study. These findings are consistent with those reported in Côte d'Ivoire and Ethiopia (Ouattara et al., 2010; Eyayu et al., 2021). These findings do not agree with other previous studies carried out in Cuban rural areas where the prevalence of soil transmitted infections was found to be higher (Pino Santos et al., 2014). Amoebiasis is the third leading cause of death worldwide especially in developing countries. Nevertheless, more than 90 % of recorded infections with E. histolytica are confusing because they are due to E. dispar not E. histolytica (Amin, 2002). The wide spectrum of amoebiasis ranges from asymptomatic infection to the development of a severe infection with amoebic colitis and even the liver may be involved and causing amoebic liver abscesses.

The results of our study showed that G. lamblia was the second most prevalent protozoan parasite in the population. This result was in line with research conducted at Agboville Area (Côte d'Ivoire), where E. histolytica and G. lamblia were the most prevalent protozoa (Ouattara et al., 2010).

In the current study, only 9.53 % of the samples tested positive for helminths, with the pinworm E. vermicularis being the most often reported helminth (8.56 %). However, their prevalence may have been underestimated since they were not diagnosed using the Graham Test. The possible reason for the low prevalence of soil–transmitted helminths: A. lumbricoides, T. trichiuria and A. duodenale) may be explained with the temperatures higher than 40°C in Iraq during summer which can limit the viability of these helminths in the environment (Brooker et al., 2006).

Regarding seasonality, the maximum peaks of intestinal parasitic infections were recorded during winter (January and February), which are rainy months in Erbil. These results are consistent with those reported by González-Moreno et al. (2011) in Spain and by Riaz et al. (2020) who reported higher infection rates in the rainy season. While the lowest prevalence was observed in March (spring). This may be due to the fact that heavy winter rains may have an impact on the spread of intestinal parasites to humans because rain wash the contaminated soil and may make it easier for parasite cysts and eggs to enter surface water.