Background
Intestinal parasitic infections (IPIs) are an important cause of morbidity and mortality worldwide [
1] affecting about 3.5 billion people globally [
2]. IPIs are endemic in resource-limited regions due to high population density, low access to improved water sources, low latrine availability, poor hygiene conditions, low health awareness, and limited economic resources [
3,
4]. Helminths such as
Ascaris lumbricoides, Hookworm
, Strongloides stercolaris and
Trichuris trichiura, and enteric protozoan parasites such as
Entamoeba histolytica, Giardia lamblia and
Cryptosporidium spp. cause high incidences of health problems especially in children in low to middle income countries [
5].
Children due to their immature immune systems and frequent exposure to unhygienic environments are at high risk for IPI including helminths [
6] and protozoa [
7]. These infections are common during the period of life most critical for physical and cognitive development, hence are linked with an increased risk of childhood malnutrition and growth deficits [
8]. Poor health in children also results in deficits in cognitive development and educational achievements [
9].
As with IPIs, anaemia remains a public health problem affecting both developing and developed countries with major consequences for human health as well as social and economic development [
10]. Globally, 2011 data indicate that 43% of children under-five were anaemic, with a higher prevalence in the developing world, specifically South Asia and East Africa, being 58 and 55%, respectively [
11]. Sub-Saharan Africa is one of the most affected regions with 54% of children under-five suffering from anaemia [
12]. The causes of anaemia include folate and iron deficiencies [
13], malaria [
14], infections (e.g., intestinal helminths), and diarrhoea [
15]. Childhood anaemia has many irreversible impacts: it impairs physical growth [
16], impairs immune function
, increases susceptibility to infections [
17] and weakens motor development leading to reduced cognitive ability [
18] and short or long term mortality in severe cases [
13].
The 2016 Demographic and Health Survey of Ethiopia (EDHS) report showed that the national prevalence of anaemia among children aged 6 to 59 months was 57% [
19], which exceeds the 40% threshold set by the World Health Organization (WHO) [
13]. The EDHS report of anaemia prevalence in the Tigray regional state (54%) is marginally below the national average (57%) [
19].
Most studies conducted in Ethiopia on the prevalence of IPIs are on school-age children. Studies conducted among pre-school age children have shown IPI prevalence up to 85.1% [
20]. Similarly, national studies on anaemia prevalence report prevalence from 32 to 37% [
21]. These studies, however, are focused on either soil transmitted helminths alone [
22] or symptomatic hospitalized children [
23], or investigated anaemia alone. Furthermore, none of the above studies used modified Ziehl-Neelsen techniques to detect
Cryptosporidium spp., the second most causative agent of diarrhea among children under five next to rotavirus [
24].
There is scarcity of data on the prevalence of IPI, anaemia, and their associated risk factors among pre-school children in the study area. However, the prevalence is expected to be high given the poverty, poor hygiene, hot/humid tropical climate and lack of access to potable water. Establishing baseline prevalence and elucidating potentially modifiable risk factors for IPI and anaemia would help public health planners, policy makers and implementers to plan and design appropriate intervention strategies to reduce associated morbidity and mortality among pre-school children.
Discussion
IPI prevalence (58%) in our study was comparable with previous reports from Pakistan 52.8% [
29] and Nigeria, 51.4% [
30], though lower than studies conducted in south Ethiopia, 85.1% [
20], Cuba, 71.1% [
31] and Malaysia, 76.5% [
32]. However, our prevalence is higher than previous similar studies conducted in east Ethiopia, 24.3% [22], south Ethiopia 4.9% [34], Amhara region, 15.5% [
33], Oromia region, 49.6% [
34], Shoa, Ethiopia 17.4% [
35] and Northwest Ethiopia 25.8% [
36]. Others have reported lower IPI prevalence in Nigeria, 13.7% [
37], Iran, 26.6% [
38]
, Uganda, 26.5% [
39], Saudi Arabia, 17.7% [
40] and Yemen, 30.9% [
41]. These reported differences in IPI prevalence might be due to the difference in parasitological methods used, geographical location, level of environmental sanitation, drinking water source, season, family education, personal- hygiene, parental socioeconomic and cultural difference of the study participants.
One explanation for the high IPI prevalence in this study could be because of seasonal variation. Data collection for our study took place during the rainy season in Ethiopia, other studies [
32,
35,
40,
42] were conducted in the dry season. Seasonal variation may be explained by increased contamination of water sources (e.g., rivers, streams, and wells) with human excreta from open defecation which is the main risk factor for diarrhoeal disease and IPIs, especially children who routinely play in the an unhygienic environment [
25]. In addition, as 77% of households in our study used unprotected water sources, the main factor for faecal-oral transmitted disease such as IPIs, this may also contribute to the high IPI prevalence.
Another possible reason for the high prevalence of IPIs in our study is the laboratory methods we employed. We used the modified Ziehl Nelson method to detect
Cryptosporidium spp., whereas the other studies except [
38,
43] did not. Furthermore, some studies isolated only the soil-transmitted helminths (STH) and not protozoa which would artificially decrease IPI prevalence [
22,
32,
33,
39].
E. histolytica, G. lambilia and
C. parvum were the most prevalent protozoan parasites in our study cohort. The high prevalence of
E. histolytica/dispar (36.1%) in our study is in agreement with previous reports [
44]. Consequences of childhood
E. histolytica infection include malnourishment, anaemia and stunted growth [
45]. However, others have reported
G. lamblia [
41,
46] and
C. parvum [
47] as the dominant parasites. The difference in prevalence of enteric protozoa may be due to differences in contamination of drinking water sources, availability of toilets, handwashing and consumption of raw vegetables of the study participants.
Helminthic intestinal parasites, particularly soil transmitted helminths (STHs), commonly infect children in low to middle-income countries. In our study, helminthic infections were identified in 104 (17.1%) of the children with
H .nana 102 (16.7%) being dominant while
Ascaris, hookworm and
Trichuris infections were very rare or absent. The low STH incidence in our study might be due to the initiation of a national deworming program, as the majority, 68.3% of the children were dewormed during the data collection time and deworming is given on a regular basis. The relatively high prevalence of wearing shoes either regularly or sometimes and low prevalence of consumption of raw vegetables may also partially explain the low STH prevalence. Besides, the prevalence of STH might also be due to differences in environmental factors such as climate, topography [
48], surface temperature, altitude, soil type and rainfall [
49].
Our study shows that dewormed children were more infected with IPIs than their counter part which appears counter-intuitive. This could be due to the fact that the prevalence of STHs, where deworming is recommended, was very small in our study. Whereas, protozoan infection where deworming is not given was the most dominant. A lower prevalence of STH compared with
H. nana has been previously reported in Peru [
50] and in Eastern Ethiopia in elementary school children receiving regular albendazole deworming treatment [
51]. This could be probably due to the fact that albendazole has little effect on
H. nana unlike
Ascaris lumbricoides,
Trichuris trichiura and hookworm [
52].
Children aged 48–59 months (PR = 1.078, p = 0.009) were more likely to be infected by IPIs compared with younger children. This likely reflects increased risk of IPI exposure from playing activity of the older, more mobile children within unhygienic external environments and hence exposed to faecal-contaminated soil.
IPIs were significantly higher in children with current gastro intestinal (GI) symptoms and in those who had diarrhea in the previous 14 days. This was similar to the report from Iran [
53]. This is due to the fact that most of the isolated IPIs in this study,
E. histolytica and
G.lamblia, are potential causes of diarrhea. Likewise, STHs are usually accompanied by current gastro intestinal (GI) symptoms.
Only a quarter of households used household water treatments, mainly chlorination and boiling. Though not statistically significant, children whose family did not treat their water were 1.2 times (
p = 0.057) more likely to be infected by IPIs. Chlorination is less expensive, less time consuming and provides residual disinfection against recontamination and significantly reduces diarrhea [
54]. However, due to the smell and taste [
55], only a few families use chlorination in our study. Similarly, due to the consumption of fuel, time, and lack of residual protection against re-contamination [
56], only a few households use boiling. Hence a cheap, point of use technology, such as solar disinfection (SODIS), which overcomes these limitation is required by such communities to tackle the consumption of unsafe drinking water.
The prevalence of childhood anaemia among pre-school children in our study was 21.6%, which is comparable with studies from south central Ethiopia, 28.2% [
57], Kenya, 25% [
58], Malaysia, 26.2% [
32], and Brazil 28.9% [
59]. Our study was, however, lower than other reports from Ethiopia, 37.3–42.2% [
60,
61], the 2016 Ethiopian Health Demographic Survey, 57% [
19], the EDHS anaemia prevalence of the Tigray regional state, 54% (19) and the WHO classification for anaemia, 40% [
13].
Likewise, studies performed outside Ethiopia have reported higher anaemia prevalence including those conducted in Brazil, 32.8% [
62], Uganda, 37.2% [
14], Nigeria, 38.6% [
63], Bangladesh, 51.9% [
64], Senegal,53.4% [
65], West Africa, 51.8% [
66], Tanzania, 47.6% [
67] and Brazil, 45.1% [
62].
Possible reasons for the variation in anaemia prevalence could be due to differences in maternal education [
57] concomitant childhood malaria superinfection [
55], family income [
58], drinking water source [
51], personal-hygiene [
68] and STH infections [
54,
57]. For example, the high anaemia rate in the studies such as Tanzania, Kenya, Senegal, Uganda, south Ethiopia, was due to concomitant malaria infection. Seasonality may have also affected the anaemia prevalence in our study as malaria prevalence is usually low during the rainy season [
69] where our data collection time was from June–August, the rainy season of Ethiopia. In addition, our study participants were from the community rather than from health institutions, and the prevalence of STH, the main cause of anaemia [
58,
70] was very low in our study.
In this study, children whose mothers were not educated were significantly anaemic compared their counter parts. This was similar with the study conducted in Tanzania [
71]. This protective benefit of maternal education could be related to an increased knowledge for adequate healthcare and nutrition for children hence its possibility for decreasing the risk of anaemia. Similarly children who eat meat were less anaemic compared to those who don’t eat meat. This was supported by a study from Israel [
72]. This is due to the fact that meat is a good source of Iron; hence without enough iron, less hemoglobin and fewer red blood cells are made, leading to anaemia. It should be also noted that anaemia has a variety of causes though 50% of all cases is caused by iron deficiency [
53]. In this study, anaemia was negatively associated with household water treatment of mothers. This is because intestinal helminths and diarrhoea, which cause anaemia [
16], can be killed with household water treatments methods [
5,
6,
54].
Limitation of the study
One of the limitations of our study was that differentiation between the morphologically identical species of Entamoeba was not within the scope of this study, as only conventional microscopy was used to detect the amoebae.
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