The prevalence of intestinal helminthic infections and associated risk factors among school Children in Lumame town , Northwest , Ethiopia

This study was conducted on prevalence of intestinal helminthes infection and their associated risk factors among school children from a rural and a semi urban setting in Lumame town, Northwest, Ethiopia. A cross-sectional parasitological study was conducted to determine the prevalence and associated risk factors of intestinal helminthes infection. A total of 402 students’ stool samples were taken and processed with direct wet mount and formalin ether concentration techniques from December to January 2011/2012. A structured questionnaire was prepared to assess the association of intestinal helminthes infection with socio-demographic and socioeconomic variables. The data collected was analyzed using  test and logistic regression (p < 0.05 was considered as statistically significant). The overall prevalence rate for at least one intestinal helminthes infection was 54.5%. Of which Ascaris lumbricoides (32.6%) was the dominant followed by hookworm (12.2%); the others were minor cases. High rate infection (A. lumbricoides) was recorded among students who had dirty finger nails, large family, habit of eating undercooked vegetable, walking barefoot, and had no latrine than their respective counterpart. Such relatively high prevalence rate of helminthes infection in the study area could be used as a baseline for the concerned bodies to launch de-worming intervention.


INTRODUCTION
Intestinal helminthes infections are among the most common and neglected public health problems in many developing countries including Ethiopia.Worldwide, more than 3.5 billion people are infected with intestinal worms (Luong, 2003), and an estimated 4.5 billion individuals are at risk of soil-transmitted helminths infection (Uneke, 2010).Majority of infected people live in resource-poor settings, 80% of these in sub-Saharan Africa (Jamison et al., 2006).Epidemiological surveys have revealed that poor sanitary conditions such as open field defecation and faecal contamination of water bodies are the most important factors leading to intestinal worm infestation, while the spread is due to lack of personal hygiene (Okyay et al., 2004;Hung et al., 2005;Abebe et al., 2001).
In Ethiopia, the prevalence and distribution of intestinal helminth infection among school children varies from place to place (Mengistu and Birhanu, 2004;Girum, 2005).Likewise, Yared et al. (2001) reported that the low economic standard, poor sanitation, ignorance of simple health promotion factors favor the wide distribution of intestinal helminth infections.Of all types of disease in the country, helminthiasis is the second most common cause of outpatient morbidity next to malaria (Yared et al., 2001).
Although several studies have been conducted on the distribution and prevalence of intestinal parasite in Ethiopia, there are still several localities for which epidemiological information is not available.One of such localities is Lumamae town.Thus, the present investigation was undertaken to determine the prevalence and associated risk factors of intestinal helminth infection, to provide recent and valuable information and to set baseline data for those who are working in the prevention and control of intestinal helminth infection among school children in the area.

Study area
Lumame is located 260 km away from the capital city, Addis Ababa with an altitude of 1850 m above sea level and an average temperature of 16.25°C.The area is predominantly rural about 89% and most residents live in villages as agriculturalists (AFEO, 2011).

Study design and period
Institution based cross-sectional study was conducted among Lumame primary school children (grade 1 to 8) from December to January 2011/2012.

Study population
The study population was students attending Lumame elementary school in 2011/2012 academic year.The total population enrolled by that academic year was 2865.

Sample size determination and sampling techniques
The sample size was determined using single population proportion formula by considering the prevalence of intestinal parasites in primary school children 95% confidence interval (CI), and design effect that give a final sample size of 422.Proportional allocation for each grade was determined and the desired sample was obtained by systematic sampling technique using the class roster formula (Daniel et al., 1999): where n = total number of sample size required, Z = Z statistics for a level of confidence (Z α/2 = 1.96), d = marginal error for 95% confidence level, p = expected prevalence of intestinal helminthes in the study area.Since, there was no previous study in the area; P value of 0.5 was taken.

Data collection and laboratory procedures
Data about the socio demographic characteristics and other associated factors were collected using a semi structured based questionnaire.Onsite training was given for interviewers.The interviewers also inspected whether they wore shoe or not.Approximately 2 g of stool specimen was collected using clean, tightly corked, leak proof containers.Small amount of the sample was analyzed using wet mount technique and the remaining portion was concentrated using formal-ether concentration technique and examined microscopically (Adefioye et al., 2011).

Statistical analysis
All statistical analysis was performed using Statistical Package for Social Sciences (SPSS) for window version 16 statistical package.
Descriptive statistics was used to present prevalence of intestinal helminth infection as percentage and proportion.The association between student's socio-demographic or socioeconomic variables and prevalence of parasitism was analyzed using Chi-square test.
Logistic regression analysis was used to determine the independent effect of the variables by calculating the strength of the association between infection and risk factors using odds ratio (OR) and 95% confidence interval (CI).P-value < 0.05 was considered as statistically significant.

Socio-demographic and other characteristics of study subjects
A total of 422 students were sampled from grade 1 to 8 in this study.Of these, 402 (95.3%) of them positively responded for intestinal helminthes examination by providing fresh stool.The age of study subjects range from 6 to 19 with mean age of 11.67 years.
Students were grouped into three age groups (6 to 10, 11 to14, and 15 to 19 years old).Age group 6 to 10 year accounts for 39.5%, while the remaining group was 40.8 and 19.7%, respectively.Students were further grouped into two grade levels (grades 1 to 4 and 5 to 8) and grade 5 to 8 group accounts for 51.2% of the study subjects.From a total of 402 study participants, 121 (30%) were from nearby rural area and 281 (70%) were urban settings.The proportion of male and female participants was nearly equal 206 (51.2%) and 196 (48.8%), respectively.
Half of student's mothers were illiterate and concerning the occupation, 42.3% students mother were housewives; the remaining, 31.3,23.2 and 3.2% earn their living as government employees, merchants and daily laborers, respectively.
More than half of the study participants (52.7%) used pipe water, while 39.6 and 7.7% used rivers/streams and well water as source of drinking, respectively.Regarding latrine availability and defecation habit, 61.4% of the study participant had latrine, and 60.7% defecate in latrine only while the rest 39.3% in open field.
Regarding shoe wearing habit, 43.5% wore shoe always, 40.1% sometimes and 16.4% not at all.On assessment about family size, 42.3% of the study subjects subjects had family size range from 1 to 3, 26.6% had 4 to 6 member and 31.1% above 6.
Concerning food habit, 37.1% of the study subjects eat raw or under cooked meat and 38.1% study subjects eat unwashed or under cooked vegetables while the remaining 62.9 and 61.9% did not such a habit, respectively.About 96% of the study subjects washed their hands before eating a meal.However, observation of the students hand cleanliness at the time of interview revealed that 32.8% of the total had dirty material in their finger nails.Furthermore, 74.1% of the study subjects did not have a habit of swimming.
Nearly half (47.8%) of the study subjects had a single helminth infections, while 5.7 and 1% had double and triple helminth infections, respectively (Table 1).The most frequent combination of helminth infection identified was co-infection of A. lumbricoides and Hook worm (3.5%), followed by A. lumbricoides and T. trichuria (1.0%) and the least being E. vermicularis and A. lumbricoides (0.5%).
There was a statistical significant association between age group, mother's occupation, family size, educational status of mothers, and availability of latrine, shoe wearing habit, defecation habit, presence or absence of dirty matter on finger nails, eating raw/unwashed vegetable with overall intestinal helminth infection (p < 0.05) (Table 2).
Helminth infection varied significantly with grade level of study subjects ( 2 =9.305, df=1, p=0.002).Grade level 1 to 4 students harbor more helminth infection, 55.7% of the total infected students than grade level 5 to 8. The overall prevalence of intestinal helminth infection with respect to age group was statistically significant ( 2 =14.827, df=2, p=0.001).Children between the age group 6 to 10 years old were more affected by helminth infection than the other age groups.Prevalence decreased in age group 11 to 14 years old and the least being 15 to 19 age groups (Table 2).

Risk factors associated with intestinal helminth infections
Risk factor analysis was performed for all variables that were significantly associated with any of the intestinal helminth infection from Chi-square test analysis.Multivariate logistic regression analysis on intestinal helminth infection showed that there was no significant difference in infection rate between grade levels, age groups, mother's education, mother's occupation, defecation  habit and source of drinking water (p > 0.05).None of these were risk factors for helminth infection in this study (Table 3).On the other hand, presence of dirty material in the finger nails was the potential risk factor (OR = 7.925 for dirty versus clean finger nails; 95% CI 3.983 -15.766).Study subjects with dirty material in finger nails were 7.925 times more likely to be infected.Similarly, the model showed that having large family was a risk factor for helminth infection (OR = 6.949 for family member >6 versus 1 to 3, P < 0.000 and OR = 4.784 for family member 4 to 6 versus 1 to 3, p < 0.000).
Regarding feeding habit, study subjects who eat unwashed or undercooked vegetables and fruit were more likely exposed to helminth infection than those who did not eat.The difference was significant (OR = 4.095 for eating versus not eating; 95% CI: 2.176 -7.704).
The model also showed that shoe wearing habit was a risk factor for helminth infection.Students who did not wear shoe were at higher risk (OR = 0.36 for those who did not wear shoe versus those who wear always; 95% CI: 0.147 -0.884).
Furthermore, the model identified the lack of latrine as a risk factor for helminth infection.The difference was significant (OR = 0.307 for none latrine versus latrine; 95% CI: 0.097 -0.973).Students who did not have latrine were 0.307 times more likely to be infected than those that had latrine.

Relationship between intestinal helminth species and some selected variables
Although, age groups, grade levels, source of drinking water and defecation habit and mother's occupation were not identified as risk factor for helminth infection.They were significantly associated with intestinal helminth infection.Except E. vermicularis and T. trichuria each helminth species identified in this study revealed significant difference with respect to age group ( 2 ).Prevalence of hookworm and Taenia spp.were significantly increased with age, whereas A. lumbricoides, H. nana and S. stercoralis significantly decreased (Table 4).
The two predominant helminth infections in this study, A. lumbricoides and Hookworm, were significantly associated with source of drinking water while the rest of the helminthes did not.Source of drinking water significantly associated with A. lumbricoides and Hookworm infection among students ( 2 = 15.928,df = 2, p = 0.000) and ( 2 = 7.81, df = 2, p = 0.02), respectively.
Study subjects who defecated in open field harbor more helminth infections than those that defecated in latrine (76.6% versus 40.2% from the total helminth infection).Defecation habit was significantly associated with A. lumbricoides and Hookworm infections among study subjects ( 2 = 16.267,df = 1, p = 0.000) and ( 2 = 9.245, df = 1, p = 0.002), respectively (Figure 2).Logistic regression analysis revealed shoe wearing as risk factors for hookworm infection.Study subjects who did not wear shoe were 3.28 times at risk of infection thanthose who wore shoe always and the difference were statistically significant.Although, the overall helminth prevalence did not differ significantly with respect to residence (Rural versus Urban), hookworm infection was significantly different between urban and rural students and being rural was a risk factor.Rural student were 3.070 times more exposed to hookworm infection than urban students (Table 5).

DISCUSSION
Studying the infection prevalence of intestinal helminthes and associated risk factors in different localities is a primary objective to identify high risk communities and select appropriate intervention mechanisms.In line with this view, the present study attempted to assess the prevalence of intestinal helminth infections and risk factors among Lumame elementary school children.This study identified seven types of intestinal helminth species.The overall prevalence of any helminth infection was 54.5% among students.This result was in line with prevalence rates reported by Teklemariam andTeklemariam (1983) andOlusegum et al. (2011).On the other hand, the present finding was higher than that reported by Girum (2005) and Anosike et al. (2006).The differences in findings among the studies might be due to variations in socio-economic conditions, individual behavioral habits of selected children, the methods employed for stool examination, the sample size taken and the time of study (Mengistu and Berhanu , 2004;Yared et al., 2001).
A. lumbricoides was the most dominant helminth infection followed by hookworm.The result was higher than school children reported by Ihesiulor et al. (2006) and Abebe et al. (2011).However, it was comparable to the reports by Lapiso et al. (2002) and Olusegun et al. (2011).Hookworm species was lower in the study conducted by Mengistu and Birhanu (2004) and Fekadu et al. (2008).But it was in line with studies Mani et al. (2002) and Anosike et al. (2006).The difference in prevalence rate of hookworm could be climate and behavior of study subjects.The relatively low prevalence of T. trichuria, H. nana, S. stercoralis, Taenia spp. and E. vermicularis, in this study was in agreement with other studies (Yared et al., 2001;Fekadu et al., 2008;Asrat et al., 2011).
In this study, the presence of dirty material in finger nails, having large family and availability of latrine were the main risk factor of A. lumbricoides infection.The result is in line with other studies (Dongre et al., 2008;Asrat et al., 2011;Olusegun et al., 2011).This is probably due to insufficient water supplies, poor hygienic practice, poor socio-economic status of the study subjects, and contamination of vegetables with fecal materials in the farm.A. lumbricoides significantly affected the age group and grade level in the study.Similar findings were reported by Awasthi et al. (2003), Fleming et al. (2006), Inabo and John (2010) and Abebe et al. (2011).This high infection rate of A. lumbricoides could be linked to the route of infection being faeco-oral, since children within this age are easily susceptible due to poor level of hygiene and indiscriminately play on fecal contaminated grounds and have a common habit of placing soiled fingers in the mouth.On the other hand, low prevalence rate among older age group and grade level 5 to 8 in this study, was possibly due to the change in attitude, habits, and more awareness regarding to personal hygiene among the older school children.
In addition, children who defecated in open field and used rivers/streams as source of drinking water harbored more A. lumbricoides infection than their respective counterparts.This result was consistent with other studies Yared et al. (2001) and Asrat et al. (2011).This is  the environment and hence favor the transmission.

Helminth species
Similarly, literacy rate of mother and mothers' occupation are found to be important helminth transmission factors.The result was in agreement with findings reported by Okyay et al. (2004) and Hung et al. (2005).This is more likely that parents of children at high level of education provide better sanitation condition for their children than low educational level parents and low level of hygiene and high exposure potentials of daily laborer mothers, respectively.
Hookworm infection, in this study significantly varied with age.This is in agreement with other studies (Anosike et al., 2006;Fleming et al., 2006).High rate of hookworm infection in older aged group probably linked to having high outdoor activities such as helping in farming, playing at the back yard in moist soil, etc., resulting in higher exposure to infective egg and filariform larvae in the soil.
In this study, students who did not wear shoe were more likely to be infected by hookworm infection than who wore shoe always.Similarly, being rural was the risk factor for hookworm infection than urban.This finding was in agreement with Lapiso et al. (2002).

CONCLUSION AND RECOMMENDATION
Intestinal helminth infections were prevalent in varying magnitude among Lumame elementary school children and were important health problem with relatively high overall rate of prevalence (54.5%).The predominant helminth was A. lumbricoides followed by Hookworm and the rest were minor cases.The relatively high prevalence rate of intestinal helminth infection in the study area might be the reflection of poor sanitation of the environment, poor personal hygiene, relatively unhygienic water supply, and others.
The presence of dirty material in finger nails was the main risk factor for intestinal helminth infection followed by having large family size, consumption of unwashed or raw vegetable, walking bare foot and lack of toilet in the study area.Therefore, personal sanitary education, having small family size, proper cooking or washing of vegetables before eating, using toilet for defecation, and always wearing shoe were important measures that greatly reduced the predominant intestinal helminth infections prevalent in the study area.
In order to reduce the impact of helminth infection among children, adequate intervention strategies should be designed and implemented.Therefore, the authors recommended that local health sector should collaborate with school health program for delivering health education to enhance the knowledge and attitude of the children against transmission of intestinal helminthes.The local government should improve pipe water supply, latrine facilities and health education to the society since A. lumbricoides infection can be significantly reduced by improving these services.
Furthermore, the current study did not address the intensity of helminth infection.Hence, further research focusing on intensity infection should be conducted for further status of helminth infection in the study area.

Figure 1 .
Figure 1.Prevalence of intestinal helminth infection in the study subjects.

Figure 2 .
Figure 2. Prevalence of intestinal helminth infections with respect to defecation habits.

Table 2 .
Association of socio-demographic and other characteristics with intestinal helminth infection.

Table 3 .
Multivariate logistic regression analysis showing the impact of selected risk factors on intestinal helminth infections.

Table 4 .
The relationship between intestinal helminth infections and age groups.

Table 5 .
The risk factors of Hookworm infection with respect to shoe wearing habit and residence.