Introduction

Most developing countries have experienced a significant decrease in child mortality rates over the last three decades (Onis et al, 2000). As greater numbers of children survive, schoolchildren face health problems such as malnutrition, anaemia and parasitic infections that compromise their physical development, school attendance and ability to learn (Bundy & Guyatt, 1996; PCD, 2000). School-based health programmes are among most of the cost-effective public health strategies (World Bank, 1993) and, school feeding programmes and treating school-aged children with anthelmintic drugs have shown improved growth and micronutrient status and higher scores in tests of cognitive function (Hall et al, 1997; Del Rosso, 1999).

Sanliurfa province is in an underdeveloped region of southeastern Turkey. While a number of studies indicate that intestinal helminth infections were endemic in the population (Ozbilge et al, 1998; Nazligul et al, 1997), there has been no data available about anthropometric status, anaemia and helminthic infections of schoolchildren in the province. For example, what are the prevalences of stunting, underweight, wasting and anaemia among schoolchildren? Are there any correlations between stunting, being underweight, wasting, anaemia and sex, type of settlement and intestinal helminth infections? These questions should be given priority in establishing the most appropriate intervention strategies to improve children's health and nutritional status. Therefore, these surveys had two aims: first, to provide baseline information about anthropometric status, anaemia and helminthic infections in schoolchildren living in different environmental conditions and second, to propose the establishment of intervention priorities in the province.

Materials and methods

Study areas

Sanliurfa province is an underdeveloped region in southern Turkey. It is at crossroads between the Mediterranean, the Anatolian plateau and Mesopotamia. It is situated on a semiarid plain at 550 m above the sea level. The area has an average temperature of 18.1°C and a minimum of -12.4°C in February and a maximum of 46.5°C in August. The average annual relative humidity is 49%, and the average rainfall is 463 mm (Turkish Government's Statistical Records Annual Report, 2000). In the province, the main industrial structure is the southeastern project (GAP), a massive dam and waterways project currently under construction. GAP has attracted many people from rural areas to migrate to the province. These people tend to inhabit shantytowns in the city outskirts, constructing mud-and-brick houses around a small central courtyard. In these areas, sanitary conditions are poor, with household liquid and rubbish accumulating in the streets. On the other hand, residents of higher socio-economic status have settled in new apartment buildings in the north of the city. In contrast to the shantytowns, the apartment areas have good sanitation conditions. The province's population number is 513 575. In all, 63.6% of the population lives in shantytowns, while 36.2% of the population resides in apartment areas (The city municipality records, 2000). A total of 74 000 children were enrolled in 44 primary schools in the urban city of the province. In all, 46 768 children (63.2%) were enrolled in 30 primary schools in shantytown districts, whereas 27 232 children (36.8%) were enrolled in 14 primary schools in apartment districts (The education administration records, 2000).

Sample design

The study was carried out in the period between January and June 2001. Multistage random cluster sampling technique was used to select the study sample (Bennett et al, 1991). In the first stage, the urban area of the province was stratified into two strata on the basis of socio-economic and environmental conditions: shantytowns and apartment areas. In the second stage, a total of 17 schools (clusters), 12 schools in shantytown areas and five schools in apartment areas were randomly selected based on the probability proportional size of each stratum. The sample size was adapted from WHO's sampling strategy in order to provide enough samples for nutritional surveys (Montresor et al, 1998). In the third stage, a third class (including 9–10-y-old children) was randomly selected in each school. The reason for this is that the peak of the prevalence and intensity of helminthic infections is found in this age group, as children of this age suffer from nutritional deficiencies and are undergoing a period of intense physical and mental development, and because experience shows that there is generally good compliance from both children and parents (Montresor et al, 1998). A total of 962 children, 650 of them from shantytown schools and 312 from apartment schools were enrolled in selected classes in the schools. The survey team distributed leaflets to these children for their parents' information and consent in selected classes. The following day, the team members checked pupils' approval and collect samples from pupils who returned with approval. They organised the survey as a flow chart while the children sat in their chairs. A child form (including the child's name, birth date, sex, height, weight, haemoglobin concentration and helminth infections with eggs per gram stool) was used during surveys.

Anthropometric survey

A portable weight and height calculator (NAN Corporation) was placed near a writing table in each classroom, and children's weights and heights were measured to the nearest 0.1 kg. Anthropometric indices were calculated using New Anthro 1.02 software (CDC/WHO, 1999), which use the NCHS/WHO international reference values. Three anthropometric indices—height for age, weight for age and weight for height—were expressed as differences from the median in standard deviation units or z-scores. These indices were calculated assuming mid-year age for each child because of doubts over the correct date of birth. Children were classified as stunted, underweight and wasted if z-scores of height for age, weight for age and weight for height were less than 2 standard deviations (s.d.) below the NCHS/WHO median.

Haemoglobin survey

Venous blood (2 ml) was drawn from each child in the selected class. The haemoglobin concentration was measured by Boehringer's cyanmethaemoglobin method using a 5110 spectrophotometer with an accuracy of 0.1 g/l. Children were classified as anaemic if the haemoglobin concentration was less than 120 g/l (WHO, 1975).

Parasitological survey

A plastic container marked with an identification number and with the name of the subject was distributed to each child. The survey team collected one stool sample from each child because the main purpose of the study was to obtain the epidemiological status of schoolchildren and it was inevitable to cover a larger scale of samples under the limitations of facilities (Hayashi, 1993). Stool samples were examined within 12 h by the semiquantative Kato–Katz technique for the eggs of intestinal helminths (Ascaris lumbricoides, Trichiuris trichiura), and the concentration of eggs was expressed as mean egg per gram ground (mepg) (WHO, 1994). Eggs of tapeworm infections (Hymenolepis nana and Taenia species) were not calculated as they excreted proglottids into faeces.

Data entry and statistical analyses

Data entry and management were carried out using the Epi-Info computer program (CDC, 1994). Statistical analyses were undertaken using SPSS for windows™ (Norusis, 1999). We used ² testing, Student's t-test and multiple regression analyses for statistical analyses. P-values of <0.05 were taken to indicate statistical significance.

Results

A total of 806 children, 572 of them from shantytown schools and 234 from apartment schools took part in the surveys. The sex distribution was significantly different between shantytown and apartment schoolchildren, with boys constituting a greater percentage than girls in shantytowns, but the genders being equally distributed in apartment schools (P<0.0001).

Children's mean anthropometric scores and haemoglobin concentrations

The mean z-scores of height for age was significantly associated with the type of settlement, in which both male and female children in shantytown schools had significantly lower mean z-scores of height for age than those of apartment schools (Table 1). These scores were also significantly associated with the sex of the children, that of the boys had significantly lower mean z-scores of height for age than the girls in both groups of schools. The mean z-scores of weight for age were significantly associated with the type of settlement, in which both male and female children in shantytown schools had significantly lower mean z-scores of weight for age than those of apartment schools. The mean z-scores of weight for height was significantly associated with the type of settlement in that boys of shantytown schools had significantly lower mean z-scores of weight for height than those of apartment schools (P<0.0001), but these scores in girls did not differ between the two groups of schools. The mean z-scores of weight for height were also significantly associated with the sex of the children in shantytown schools, that of the boys had significantly lower mean z-scores of weight for height than girls (P: 0.02), whereas these scores did not differ between sexes in apartment schools. The mean haemoglobin concentrations were significantly associated with the type of settlement, in which both male and female children in shantytown schools had significantly lower mean haemoglobin concentrations than those of apartment schoolchildren.

Table 1 - Variations of mean z-scores height and weight for age, weight for height and mean haemoglobin concentrations according to sexes in shantytown and apartment schools.

Full table

Children's undernutrition and anaemic rates

Stunting was significantly associated with the type of settlements in that both boys and girls in shantytown schools had significantly higher stunting rates than those of apartment schools. (Table 2). Stunting was also significantly associated with the sex of the children in shantytown schools, that of the boys had significantly higher stunting rates than girls (P: 0.002), but this rate did not differ between sexes in apartment schools. Underweight did not significantly differ according to the type of settlements. However, underweight was significantly associated with sexes in shantytown schools, that of the boys had significantly higher underweight rates than girls (P: 0.04). But these scores did not differ between sexes in apartment schools. Wasting was significantly associated with the type of settlements, in which the girls in apartment schools had significantly higher wasting rates than those of shantytown schools (P: 0.02). The prevalence of anaemia was significantly associated with the type of settlements in which both male and female children in shantytown schools had significantly higher anaemia rates than apartment schools (P: 0.01) (Table 2).

Table 2 - Variations of the prevalence of undernutrition and anaemia according to sexes in shantytown and apartment schools.

Full table

Children's intestinal helminth infections

The prevalence of intestinal helminthic infections was significantly higher in shantytown schools than apartment schools (P<0.0001) (Table 3). The prevalence and mepg (mean eggs of per gram stool) of Ascaris, Trichuris and H. nana infections were significantly higher in shantytown schoolchildren than apartment schoolchildren (P<0.0001). But the reverse was true in Taenia infections; its prevalence was significantly higher in apartment schools than shantytown schools (P<0.0001).

Table 3 - Prevalence and intensity of each kind of helminth infections according to sexes in shantytown and apartment primary schools.

Full table

This survey also analysed the relationship between anthropometric scores and helminth infections. Helminthic infections in children were significantly related to stunting in shantytown schools (multiple R=0.147; P: 0.005) and apartment schools (multiple R=0.171; P: 0.02). Infection in children was not significantly related to underweight in both study areas. Infection in children was also not significantly related to wasting in both groups of schools.

Discussion

This survey provided baseline data about anthrometric indices, anaemia and intestinal helminthic infections of schoolchildren living in better and worse socio-economic and environmental conditions in the Sanliurfa province of Turkey. The evidence shows clearly that most of the schoolchildren in shantytown schools experienced poor health due to undernutrition, anaemia and intestinal helminthic infections. These health problems lead to chronic ill-health in children and affect their cognitive development, with a consequence of not developing skills and the ability for future prospects (Nokes & Bundy, 1994). However, the schoolchildren living in better socio-economic conditions experienced a low prevalence of chronic undernutrition, anaemia and helminthic infections, leading to better health and education outcomes in the apartment community.

The data clearly indicated that the mean z-scores of height for age was significantly lower in boys than girls in both groups of schools confirming other cross-sectional studies in Ghana and Tanzania, Vietnam and Indonesia (PCD, 1998a, 1998b). Although the boys had a higher stunting rate than girls in shantytown schools, in apartment schools, they did not. It is suggested that growth in boys may be more sensitive to environmental insults such as infections and diseases (Parraga et al, 1996). Previous studies reported that diarrhoeal diseases, amoebal dysenteric diseases and enteric fever infections were prevalent in the shantytown community (Ulukanligil et al, 2001a, 2001b). These infections might account for the high levels of undernutrition rates observed in the shantytown schoolchildren.

The data also indicated that the children in shantytown schools had lower mean z-scores of height for age and higher stunting rates than those of apartment schools. These results were confirmed by other studies indicating that parasitic diseases or the unavailability of food, insufficient purchasing power, inappropriate distribution and inadequate utilisation might make the children vulnerable to stunting in a deprived community (Onis et al, 2000; PCD, 2000). The majority of populations in the shantytown community are seasonal labourers of low socio-economic status (Gurel et al, 2002). Whole families, including the father, mother and children participate in seasonal labour between June and October. They usually work in cotton plantations in the Cukurova region, returning to Sanliurfa in the winter (Gurel et al, 2002). Poverty, ignorance, low purchasing power and poor living conditions and their consequences of stunting, underweight, anaemia and parasitic infections together produce a vicious cycle in the shantytown community. This cycle can be broken with the establishment of school health programmes that included deworming, feeding and micronutrient iron supplements through health education, with potentially beneficial effects on the children's health and education. This development may create capacity building and skills in younger generations throughout their formal education, which may create productivity and employment prospects with implications for the economic development of this deprived community. In addition, school health programmes can involve the community in the deworming and feeding activities, which may increase their awareness about the importance of health and education, and subsequently the adults may become more active in challenging poverty and ignorance.

The data indicated that both male and female schoolchildren in shantytown schools had significantly lower mean z-scores of weight for age than those of apartment schools. This result might be due to the lower socio-economic status of shantytown community and can reflect a broad range of insults such as poverty, ignorance, large family size and inadequate utilisation at the house-hold level in slum dwellers (Kan, 1993). The data also indicated that the boys were thinner than girls in shantytown schools conforming to the study that indicated that the boys were more vulnerable to chronic unfavour-able conditions such as infections or disease (Parraga et al, 1996).

The data indicating that the relatively low prevalence of wasting showed that a recent and severe process of weight loss was not widespread among schoolchildren at the time of the survey. But the prevalence of wasting was significantly higher in children in apartment schools than those of shantytown schools (P: 0.02). Wasting is often associated with acute starvation or severe disease (WHO, 1997). Acute starvation was not expected in apartment schoolchildren and it might be due to the fact that wasted children suffered from severe disease at the time of the survey.

The data also highlighted that high prevalence of anaemia in shantytown schools (45%) constituted public health priority and necessitated urgent intervention. Many studies reported that childhood anaemia is likely to be due to poor nutrition (deficient for iron) and helminthic infections (partially Hookworm and Trichuris) (WHO, 1975; Stephenson, 1994). It can be alleviated by the treatment of intestinal helminths and by micronutrient iron supplements, which could be delivered in a simple health package through school health programmes (Hall et al, 1997).

The data also showed the prevalence of intestinal helminthic infections in shantytown schoolchildren (63%). It might be due to poor environmental sanitation and poor living conditions existing in shantytown districts. The data also showed that the prevalence of Ascaris, Trichuris and H. nana infections was higher in shantytown school children than in apartment schoolchildren, except that Taenia infections were significantly higher in children of apartment schools than those of shantytown schools (P<0.0001). This may be due to the fact that the population has the habit of eating raw meat (mixed with bulgur wheat and hard pepper), which increases the risk of acquiring scolex of Taenia species. The data also showed that intestinal helminth infections were significantly related to stunting in both groups of schoolchildren. This result was confirmed by several studies that indicated that undernutrition is one of the most common sequences of infection with A. lumbricodes, T. trichiura and Hookworm (Stephenson, 1994) and is also strongly associated with deficits in mental functioning (Simeon & Grantham-McGregor, 1990). These results also indicated that targeted treatment was warranted and a broad-spectrum benzimidazole (albendazole or mebendazole) will treat at least 60% of children infected with Ascaris and Trichuris. These effective and inexpensive treatments can be readily delivered to the schools at a low cost (PCD, 1997; Albonico et al, 1999). The expected benefits of deworming include growth, appetite, fitness, cognitive performance and iron stores (Nokes & Bundy, 1994). The prevalence of tapeworm infections did not exceed 12% in schoolchildren and their treatment could be delayed until the prevalence of overall helminth infections declined to a certain level, in which case management would be more advantageous (Bundy et al, 1990).

The surveys have certain limitations with respect to the inaccuracy of children's dates of birth, which affect z-scores of height and weight for age. Since most of the children's birthdays were 1 January according to their school's records and the children did not know their exact birth date during their interview, we took a mid-year date of birth under these circumstances. However, the surveys provided baseline data about anthropometric status, anaemia and helminthic infections in schoolchildren. These data strongly support the need for school health programmes aimed at improving undernutrition and anaemic conditions and reducing the prevalence of infection in schoolchildren, with potentially beneficial effects on educational outcomes.

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Acknowledgements

These surveys were undertaken by the grants of Harran University Research Foundation in Sanliurfa, Turkey.