Anthropometric Status , Anemia and Intestinal Parasitic infections among Primary School Children in Alexandria , Egypt

BACKGROUND: In developing countries, malnutrition is a major health problem with prevalence ranges of 4-46%. Early childhood malnutrition is irreversible and intergenerational, with adverse consequences on adult health. OBJECTIVES: This study aimed to determine the current prevalence and some associated risk factors of anemia, anthropometric indices and intestinal parasitic infection among primary school children in Alexandria, Egypt. METHODS: A cross sectional study was carried out on 330 school children aged 6-12 years, attending governmental primary schools, in Alexandria. The sample was selected using a multistage random cluster sampling technique. Nutritional status of these children was determined using age and the anthropometric parameters of weight and height. z-scores of height-for-age, weight-for-age and weight-for-height were computed. Epi Info 2000 software was used to evaluate the anthropometric results of each individual. Cyanmethaemoglobin method and two Kato thick smear technique were employed to identify blood hemoglobin and parasites respectively. Data were analyzed using appropriate descriptive, univariate and multivariate logistic regression methods. RESULTS: Underweight, stunting, wasting, anemia and intestinal parasitoses were 4.2%, 3%, 3.7%, 84.5% and 33.6 % respectively. Parasites encountered during the study were Ascaris lumbricoides (24.6%), Trichuiris trichiura (19.6 %), and Enterobius vermicularis (3%) respectively. Based on multiple logistic regression analyses, the main risk factor for stunting was the presence of parasitic infection (OR = 4.85; 95%CI=1.23-19.12). The risk factors for anemia were age ≥10 years (OR = 8.79; 95% CI = 2.0138.35), and presence of parasitic infection (OR= 2.26; 95% CI = 1.074.82), while the risk factors for parasitic infection were age 8 -10 years (OR = 1.94; 95% CI = 1.13 3.34; P = 0.02),and age ≥10 years (OR = 1.99; 95% CI = 1.05 3.79; P = 0.035), anemia (OR= 2.1; 95% CI = 0.994.44; P = 0.054) and stunting (OR = 4.33; 95% CI = 1.05 17.83; P = 0.042). CONCLUSION: Findings from this study are strongly suggestive that intestinal parasitic infections and malnutrition exist in school children residing in Alexandria and constitute a major health problem that needs to be addressed immediately to reduce morbidity and mortality.


INTRODUCTION
School children face many health problems such as malnutrition, anemia and parasitic infections that compromise their physical development, school attendance and ability to learn.
(1) Those problems constitute a major health burden in developing countries, with infants and children being the most vulnerable Bull High Inst Public Health Vol.42 No.1 [2012]   groups.
(2) Indicators of malnutrition include wasting, stunting and being underweight.
Stunting or low height-for-age (HAZ), is thought to be a good indicator of malnutrition and represents a status of chronic nutritional stress. (3) The World Health Organization had estimated that the overall prevalence of stunting has fallen in developing countries (5) It was estimated that 30% of the world's total population are anemic. (6)In Egypt, nearly 50% of all school aged children are anemic. ( In endemic areas, school age pupils suffered from the greatest burden of parasitic infections.The disease burden is mainly manifested as nutritional stress and associated with poor appetite, food indigestion, malabsorption, impaired growth and anemia. (8)The intensity and type of parasitic infection contribute to its effect on nutrition. (9) The synergistic occurrence of helminthiasis, anemia and malnutrition exert a negative effect on growth and development of the affected person. (10) To our knowledge, malnutrition and anemia exist in school children residing in Alexandria Governorate, as elsewhere in Egypt, and constitute a major health problem that needs to be addressed immediately to reduce morbidity and mortality. (11)Few studies were carried out to study the nutritional status and parasitic infections among that age group in Egypt.
That is why the aim of this study was to determine the current prevalence and some associated risk factors of anemia, anthropometric indices and intestinal parasitic infection among primary school children in Alexandria, Egypt.

Study design and setting
A cross-sectional survey was carried out in Alexandria governmental primary schools, Egypt; from September to November 2011.

Study population, sample size and sampling technique
The study population consisted of school children aged 6 -12 years.The sample size was calculated using Epi-Info.
Based on an estimated prevalence of 50% (that gives the maximum sample size), a 95% confidence level, an 8% degree of precision and a design effect of 2, the minimum required sample size was found to be 301 and was rounded to 330.To ensure that the sample size is big enough to detect a significant effect, a power analysis was conducted with program G.
Power for each of the studied outcome measures (anaemia, stunting and parasitc infection) was done and was found to be above 80% which is sufficient to detect a significant effect.For example, to study infection as a risk factor of anemia, assuming that 30% of the sample were infected and that prevalence of anemia among those infected and those non infected was 90 and 75% respectively, the power was found to be 90%.To study infection as a risk factor of stunting, assuming that 30% of the sample was infected and that prevalence of stunting among those infected and those non infected was 10 and 2% respectively, the power was found to be 84%.

Sample characteristics
A Wasting and underweight showed no significant difference.Children who were infected had significantly lower mean hemoglobin concentration compared to those who had negative infections (10.37 g/dL compared to 10.76 g/dL; P = 0.000).Also the children who had infections were more anemic (91%) compared to those who were not infected (80.6%), the difference was statistically significant (P = 0.024).In addition, there was a significantly higher percent of higher grades of anemia among infected group (29.7%) compared to 17.3% among non-infected group (P = 0.009).
Regarding the type of parasite, 29%, 40%, and 35.4% of infected school children had moderate grade of anemia caused by Ascaris, T. trichiura, and Entrobious vermicularis, so we could conclude that T.
trichiura showed higher grades of anemia than Ascaris lumbricoids and entrobious vermicularis (Figure 2).(Table 6) In Egypt, the overall prevalence of stunting among primary school children aged 6-12 years is 11.6 %.

Figure (2) Parasite infection and grades of anemia
( This result disagrees with that found in the present study, as a lower percent of stunting was recorded (3%).This finding could be attributed to the setting of the study where Alexandria was not included in that national survey.
Meanwhile, the present findings were consistent with the results of a previous study conducted among school children. ( It was estimated that up to half of schoolaged children in developing countries are anemic. (21)The findings of the present study indicated that 84.5% of all examined subjects were anemic.This is in agreement with the results obtained in a previous study among primary school children in Egypt. (22)A similar prevalence was reported elsewhere. ( The high prevalence reported in this study could be related to high rate of parasitic infection and poverty among the study population which contribute to poor access to good diet, and proper healthcare.These results are inconsistent with the findings of Barduagni et al. (24)   , who reported that among school children from 6-11 years of age living in Upper Egypt, the prevalence of anemia is low and its severity is moderate.This may be due to low prevalence and moderate intensity of intestinal helminthic infections in this region that have been reported in a former study. ( Parasites may affect the intake of food; its subsequent digestion and absorption, metabolism and the maintenance of nutrient pools. (26)In the present study, parasitic infections influenced children's anemic status, and there was a significantly higher percent of anemic school children among the infected group.
In addition there was a significant difference between the mean hemoglobin level and that of non-infection group (p < 0.05).The mean values of all anthropometric measurements were lower in helminth-infected children.These findings were in accordance with that reported by CasapẴa et al. ( The present study showed that age >10 years was a significant risk factor for anemia among these school children.This is inconsistent with the findings demonstrated by Calis et al (28) who reported that the pre-school and early school age children had a higher risk of anemia than children over10 years.It is also inconsistent with the findings of a previous study which demonstrated that the prevalence of anemia decreased significantly with age. (29)This may be due to higher The presence of parasitic infections especially Ascaris infection was also found to be significantly associated with anemia among these subjects.The association between anemia and intestinal parasites has been previously reported. (22,30) However, in a previous study, (29) no association was found between anemia and parasitic infections, probably due to the very low prevalence of parasitic infections.Although ascariasis is known to influence the nutritional status, its impact on anemia is less clear. (31)The worms may ingest proteins and vitamins from their hosts. (32)The strong association between poverty and poor dietary intake.As a limitation, the present study did not measure the daily iron intake.However, a previous study had shown that the daily iron intake by Egyptian primary school children was only 22% among male children and 13% of females got more than 75% iron RDA.(33).
The evidence showed clearly that most of the studied school children living in poor socio-economic conditions experienced poor health due to undernutrition and intestinal parasitic infections.However, higher socioeconomic status was found to be significantly associated only with anemia among examined subjects (may be due to poor dietary choices, eating less nutrient dense foods but energy dense foods).
One of the largest studies of rural school children in low income countries (Ghana, Tanzania, Indonesia, Vietnam and India) found that the overall prevalence of stunting in all five countries, ranged between 48% and 56%.In all countries, there was a trend for height-for-age to decrease with age, thus as children got older they became shorter and boys in most countries tended to be more stunted than girls. ( The present investigation revealed that children below the ages of 10 years were less stunted compared to those ≥10 years, but this did not reach statistical significance (borderline p= 0.057).This is in agreement with previous similar studies. (27,35) Peru, China, (36) and Tanzania (37) .
Parasitic infections are associated with decreased appetite and low food intake, which result in decreased growth rate.
Moreover, micronutrient losses and nutrient malabsorption due to ascariasis and bloodloss due to Trichuriasis can lead to iron deficiency anemia and poor growth rate.(38)   Our results were in accordance with some studies done in many countries which proved that parasitic infections were associated with stunting in school age children. (39,40)On the other hand, Kandeel in1998 (41) did not find any effect of parasitic infections on children' growth, but he attributed this to the recent, light intensity of infection or infection for a short period.
Whoever, this finding is inconsistent with Tadesse G study in 2005 (42) where the overall prevalence rate of intestinal helminthic infections was not different among children with or without stunting and this may be attributed to the low prevalence of parasitic infection among those children.
On the other hand, due to the cross sectional design of the study, ones cannot be certain whether the infection itself increased the risk for stunting or whether the state of chronic malnutrition increased the susceptibility for acquiring the parasite.
The relationship between malnutrition and infection has been found to be synergistic. ( The combined effects observed when both malnutrition and infection are present at the same time are far more serious than the additive effects resulting when they occur separately.In other words, infections worsen cases of malnutrition and malnutrition worsen the severity of infectious diseases. As regards the overall percent of intestinal parasitic infections observed in the present work, it was found that 33.6% of the studied school children had infection.This was similar to findings of El-Masry et al who reported a prevalence of 38.5%. (45)However, the present result was less than that reported in Upper Egypt by El-Gammal et al. (46) who reported that the prevalence of parasitic The present work revealed that stunting and presence of anemia were significant risk factors of parasitic infection among those children.This is consistent with the findings of Sorensen et al. (48) Usuanlele et al (20) found no significant associations between anemia and infection categories or status and none was found too with the growth indices, probably because of the few cases of anemia.With respect to personal characteristics and risk factors, we noticed that age groups 8-10 and >10 years were risk factors.This agreed with the findings of El-Masry et al in Sohag in 2007 (45) yet contradicting the study of of Yassin et al in Gaza city in 1999 (49) who noted that G.

Conclusions and Recommendations
The main conclusion that emerged from the present study was that intestinal parasitic infections and malnutrition exist in primary schoolchildren residing in Alexandria and constitute a major health problem that needs to be addressed immediately to reduce morbidity and mortality.Parasitic infection is significantly associated with anemia and malnutrition, and the severity of subtle morbidity is significantly related to the worm from 47% in 1980 to 33% in 2000.Stunting in school age children is common in developing countries with the stunting prevalence being higher in primary schools.Malnutrition in Egypt is increasing after steady decrease in the prevalence of stunting that Egypt has experienced from the late 1970s till 2000. (4)The situation is likely to have further deteriorated since the continuing political instability following the Egyptian revolution at the start of 2011.Parasitic infections, anemia and malnutrition are prevalent and of public health concern especially among the low income groups living in rural areas in Egypt.According to the nutritional survey conducted by Tawfik in 2004 among school age children (6-12years), the prevalence of stunting was 11.6%.

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Public Health Vol.42 No.1 [2012] moderate to heavy intensity ≥5000 EPG.Calculation and scoring of socioeconomic level was based on the Modified Social Score for family social leveling (Modified by Fahmy and Sherbini 1983). (18)The social levels were then classified as: Data analysis was performed using the SPSS software version 17.0 for Windows (SPSS, Chicago, IL, USA).The distribution of quantitative data was examined using the Shapiro-Wilk test and was found to be normal.The independent t-test was used to examine the difference in Hb, weight and height between groups (infected and non infected children).Chi-squared test or Fisher's exact test whichever appropriate was used to examine the differences for proportions of anemic, stunted, underweight and wasted among infected and non-infected children.Univariate logistic regression analysis was used to identify the independent variables significantly related to the outcomes (anemia, stunting and parasitic infection) among the studied children.Crude odds ratios (ORs) and 95% confidence intervals (CIs) were calculated.All variables found to be significant were then included in stepwise multiple logistic regression analysis.The final model was interpreted by using adjusted ORs and 95% CIs.The level of significance of 0.05 was used for all the statistical tests.Ethical considerations: There were no conflicts of interest.This work received no specific grant from any funding agency in the public, commercial or not for profit sectors.This study was conducted according to the guidelines laid down for medical research involving human subjects and was approved by the Ethics Committee of the High Institute of Public Health, Alexandria University, Egypt.All measurements were taken and kept confidential.School children and their parents were informed about the objective of the study and had the right to accept or refuse to participate.An informed written consent was taken from their parents.
prevalence of parasitic infections among older age presented in present study.This finding indicates that there is a need for evaluation of the current routine iron supplementation program and deworming programs by the Ministry of Health in primary health care centers and in non-governmental organizations (NGOs) for school children.
anemia and Ascariasis observed among these children unexpectedly appeared with light intensity of infections and this may be due to presence of other contributory factors such as Bull High Inst Public Health Vol.42 No.1 [2012] infections among Egyptian school children in Demo villages was 88.5%.Rim et al(47)   collected 29,846 stool specimens from Bull High Inst Public Health Vol.42 No.1 [2012]   primary school children in Laos and the cumulative egg positive rate for intestinal helminthes was 61.9%.These findings were also relatively lower than those previously reported among different regions in Egypt (66%).(22)The high prevalence could be due to the place and living standard of study subjects or due to a reflection of the local endemicity and geographic condition of the study area.
lamblia as the most frequent (62.2%) parasitic infection followed by Ascaris lumbricoides (20.1%) and E. histolytica (13.3%) among young children .This could be attributed to examination of the stool specimens by different tests (direct smear microscopy, zinc sulphate flotation, formol ether sedimentation scotch tape and Kato Katz techniques) which enabled detection of all parasitic infections unlike our study that used only Kato Katz technique that hardly detect the protozoal infections

Table1: Distribution of the studied sample according to nutritional characteristics and parasitic infection.
□■ Chi-square or Fisher's exact test whichever appropriate □ Independent samples t test @ n = 273 where 57 school children had height > 145 cm for ♂ or > 137 forChildren's parasitic infectionResults showed that 33.6% of studied school children were infected with parasites.The prevalence of parasitic infections such as Ascaris lumbricoids,Entrobious vermicularisand Trichuris trichura infections were 24.8%, 3% and 19.6% respectively (Figure2).Among those, about a quarter of the infections by Ascaris lumbricoides and 3.1% of those by Trichuris trichiura were of moderate to heavy intensities.(Table2)