countries, 206 million children are stunted, 50 million are wasted, and 167 ... The results showed that 50 per cent of the subjects were infected with at least one ...
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Effect of Giardia Infection on Growth and Psychomotor Development of Children Aged 0–5 Years by Z. Simsek,a F. Yildiz Zeyrek and M. A. Kurcera a Public Health Department and bMicrobiology Department, Faculty of Medicine, Harran University, Sanlıurfa, Turkey
Introduction Among children under 5 years of age in developing countries, 206 million children are stunted, 50 million are wasted, and 167 million are underweight due to lack of food and the presence of diseases.1 Optimum health for children has long been known to be related to physical, socio-cultural, economic, and environmental factors.2 In developing countries, the incidence of giardiasis is often over four times higher than the 7.4 per cent incidence reported for industrialized countries.3 Children between 6 months and 5 years of age are the most susceptible population, where an incidence up to 35 per cent has been found.4 These infections, especially Giardia intestinalis, are regarded as a serious public health problem, as they cause irondeficiency anaemia, micronutrient deficiencies, protein–energy malnutrition (PEM), and growth retardation in children, associated with diarrhea and malabsorbtion syndrome.5–10 However, published evidence has not been entirely consistent regarding Acknowledgements We would like to express our special thanks and gratitude to families and children.We owe a special dept of gratitude to Health School’s professionals (Fatma Ersin, Fatma Gözükara and Miyaser Kayahan) and Tilfindir Primary Health Care Center’s team whose untiring efforts and devotion made possible the successful implementation of the survey. Correspondence: Z. Simsek, Harran University, Faculty of Medicine, Public Health Department, Denisehir Campus, Sanlıurfa, Turkey. E-mail .
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the impact of giardiasis on psychomotor development. It was, therefore, decided to investigate the consequences of Giardia on growth and psychomotor development status. Materials and Methods This cross-sectional survey was carried out within the catchment area of the Tilfindir Primary Health Care Center in the Sanliurfa district of south-eastern Anatolia, Turkey. The study was conducted during April–May 2002. From the health center’s records in the defined area, 164 children between 6 months and 5 years of age were randomly selected. The children enrolled in this study were visited in their homes. After explaining the aim of the study, informed consent was obtained from the children’s parents or caregivers. Thereafter, physical and psychomotor development examinations were carried out on each subject and fecal samples collected. Children diagnosed with intestinal parasites were given the appropriate anti-parasitic treatment. Those identified with other medical conditions were given written referrals to the Health Care Center. Poor families were also referred to the Social Services. Data collection In order to assess the association between psychomotor development and Giardia infection, the Ankara Child Development Screening Inventory (AGTE) was used. This was developed by Savasir,
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Summary Giardiasis, an intestinal protozoan infection caused by Giardia intestinalis, is common in southeastern Anatolia, Turkey. In this cross-sectional survey, to investigate the role of giardiasis on growth and psychomotor development, we studied 160 children aged 0–5 years. Data were collected using a structured questionnaire, anthropometry, Ankara Developmental Screening Inventory, and laboratory analysis of fecal samples. The results showed that 50 per cent of the subjects were infected with at least one pathogen of intestinal parasitic infections. Giardia intestinalis was the most frequent pathogenic parasite. Giardia-infected children had a risk for stunted (OR = 7.67, 95 per cent CI = 2.25–26.16; p = 0.001) and poor psychomotor development (OR = 2.68, 95 per cent CI = 1.09–6.58; p = 0.030). The data indicate that Giardia intestinalis infection has an adverse impact on child linear growth and psychomotor development. In the primary healthcare centers, during the programme of the monitoring growth and developmental status of children, following children in terms of Giardia, diagnosis and treatment will have a positive effect on child health.
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TABLE 1 Association between intestinal parasitic infection and child growth status Parasite
No Giardiasis Others
Height-for-age below –2SD ——————————— n % 11/80 26/45 6/35
13.8 57.8 17.1
Total
43/160
26.9
2 p
30.56
0.0001
Weight-for-age below –2SD ——————————— n % 3/80 9/45 2/35
3.8 20.0 5.7
Weight-for-height below –2SD ——————————— n % 2/80 2/45 0/35
Total ————————————— n %
2.5 4.4 0
80 45 35
50.0 28.1 21.9
160
100.0
14/160
8.8
4/160
2.5
10.04
0.007
1.59
NS
NS, not significant.
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the second. The samples were covered with a coverslip and systematically observed at low (10) and high magnifications (40) with a light microscope in order to identify the presence of mature parasites, cysts or eggs. In addition to these, a structured questionnaire with open- and close-ended questions, which was developed by researchers, was used for the collection of socioeconomic, environmental, and demographic data about the children. Data analysis was carried out using SPSS statistical package. Association of factors with giardiasis and other intestinal parasites and psychomotor development and growth was tested using the 2 test in univariate analysis. Logistic regression was done to find out ‘independent’ effects of demographic, social, and environmental factors on growth and psychomotor development. Results The study sample comprised 164 participants aged between 6 and 60 months and the response rate was 98 per cent for AGTE, questionnaire, anthopometry and stool samples. The mean age was 25.9 ± 15.2 months, the median was 22.5 months, and 51.3 per cent were male. Eighty children were infected by intestinal parasites: 46.7 per cent were G. intestinalis, 41.9 per cent were Enterobius vermicularis, 8 per cent were Ascaris lumbricoides, 1.9 per cent were Entamoeba histolytica, and 1.9 per cent were Trichuris trichiura. Protozoan infections were common with G. intestinalis. Among the 160 children who participated, 26.9 per cent of them were stunted, 8.8 per cent were underweight, and 2.5 per cent were wasted. Table 1 indicates that children infected with G. intestinalis were significantly stunted and underweight compared with the other parasites and non-infected children. As seen in Table 2, only giardiasis were associated with a significantly increased risk for stunting (OR = 7.67, CI = 2.25–26.16). No significant association was 91
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Sezgin and Erol and was a culturally relevant device that would yield an index of developmental status of children. AGTE is a measurement tool that evaluates ‘general development, cognitive language, fine motor, gross motor development, social and self help skills’ of children between 0 and 6 years of age. AGTE has high correlation with Denver Developmental Screening Inventory. This inventory consisted of 154 items answered by mothers as ‘yes’ or ‘no’. If a child received a score of 20–30 per cent lower than the average age level from at least two sub-tests, then s/he was classified as having poor psychomotor development.11–13 In order to assess the association between nutritional status and Giardia infection, we obtained weight and height information for all children. Weight was measured using a calibrated spring scale (0.5 kg scale), and height was measured using a supine measuring board (0.1 cm scale). Height measurements were done in babies younger than 2 years old when they were lying down, and the height of older children was measured in the standing position. Weight-for-age, height-for-age, and weight-for-height measurements were calculated using the EPINUT program of Epi-Info. This compared the subject’s measurements to international National Center for Health Statistics (NCHS) growth reference curves. The cut-off point used to identify malnourished children was less than –2 standard deviation units (SD) below the NCHS reference median. Children whose weight-for-height, height-for-age, and weightfor-age fell below –2 SDs were classified, respectively, with acute malnutrition (wasting), chronic malnutrition (stunting), or global malnutrition.14 The parents were asked to collect a stool sample from their children early in the morning after the day of assessment and this was analysed for the presence of intestinal parasites. After gross examination of fecal sample characteristics, a direct wet smear was prepared by emulsifying 2 mg of feces on a glass slide. A drop of Lugol’s solution was applied to the first half of the split sample and isotonic solution to
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TABLE 2 Factors associated with the risk for stunting
OR
95% CI
0.215 0.512 0.018 0.990
1.06 1.00
0.65–1.85 0.97–1.02
10.609 0.001
7.67
2.25–26.16
–0.499 0.511 0.771 0.406
0.60 2.16
0.13–2.68 0.35–13.32
0.632 0.177 0.560 0.234
1.88 1.75
0.75–4.71 0.69–4.40
0.117 0.873
1.12
0.26–4.74
Hosmer–Lemeshow (p = 0.782).
found with child gender, age, number of siblings, birth space, no hand-cleaning system, or education of parents. Nearly 16 per cent of children in the sample had language-cognitive delay, 17.5 per cent of children had fine motor development delay, 9.4 per cent had gross motor development delay, and 10.6 per cent of children had social skills-self care development delay. Table 3 indicates that there was a significantly relation between giardiasis and poor language-cognitive and fine motor compared with children with other parasites and healthy children. However, no significant associations were identified between gross motor and social skills-self care delay and G. intestinalis. Table 4 shows the results of the bivariate analyses that investigated the risk for the low psychomotor development. As indicated, giardiasis (OR = 2.68, CI = 1.09–6.58), above the age of 24 months (OR = 3.45, CI = 1.48–8.03), stunting (ORE = 3.60, CI = 1.60–8.08) and inferior hygiene, as reflected by no
Discussion We found that half of the study population was infected by intestinal parasites, with G. intestinalis the most common. This finding is consistent with other studies conducted in developing countries and in different geographical area of south-eastern Anatolia.15–17 In the present study, the children with Giardia had significantly poorer growth with stunting and wasting than children with other species. The relative odds of low height-for-age are about 7.7 times higher among children with giardiasis. Several authors have reported significant reductions in the linear growth of Giardia-infected children.3–6,9,18 In contrast to these findings, some authors have reported the lack of a significant association between giardiasis and stunting in young infants19 or older children.20 While differences in study design and methodology may be responsible for some of these between-study discrepancies, population differences in infection intensity and burden, and nutritional status, may be relevant. Only one study has been published which documents the intestinal parasite associated with psychosocial development. Oberhelman, et al.,9 have reported significant association between language development and infected children with Trichuris. This is the first study to examine directly the relation between psychosocial development and giardiasis. The odds of having poor psychomotor development are about three times higher among children with giardiasis, about 3.4 times higher among children older than 24 months, almost three times higher among children living at home and having no
TABLE 3 Association between intestinal parasitic infection and psychomotor development Parasite
Fine motor development ——————————— n %
Gross motor development ——————————— n %
Social skills self-care ————————————— n %
No Giardia Others
7/80 14/45 5/35
8.8 31.1 14/3
10/80 14/45 4/35
12.5 31.1 11.4
6/80 6/45 3/35
7.5 13.3 8.6
5/80 7/45 5/35
6.3 15.6 14.3
Total
26/160
16.3
28/160
17.5
15/160
9.4
17/160
10.6
1.18
0.55
3.25
2
p
92
Languagecognitive ——————————— n %
10.70
0.005
8.05
0.018
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Gender (girls) Age (above 24 months) Children with giardiasis Number of siblings Birth space (under 24 months) No hand-cleaning system after toilet Education of mother (years) Education of father (years)
p
hand-cleaning system after toilet (OR = 2.63, CI = 1.15–5.98), were associated with a significantly increased risk for psychomotor development delay. No significant associations were identified between psychomotor development delay and child gender, number of siblings, birth space, or education of parents.
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TABLE 4 Factors associated with the risk for psychomotor development Gender (girls) Age (above 24 months) Children with giardiasis Low height-for-age No hand-cleaning system after toilet Education of mother (years) Education of father (years)
p
OR
95% CI
–0.272 0.425 1.240 0.004
0.76 3.45
0.39–1.80 1.48–8.03
0.989 0.030
2.68
1.09–6.58
1.282 0.002 0.969 0.021
3.60 2.63
1.60–8.08 1.15–5.98
0.127 0.730
0.88
0.42–1.80
0.034 0.732
1.23
0.78–1.03
hand-cleaning system, and 3.6 times higher among children having low height-for-age. Giardiasis appears to play an important role in the psychosocial development delay, especially on language-cognitive and fine motor development. Some studies have been suggested that giardiasis may cause nutrient malabsorption and other adverse changes.3–6,8–10,18 The resulting delays in psychomotor development may be exacerbated where malnutrition is already present. The present study did not allow for the definitive determination of whether infection itself augmented the risks for psychomotor development or malabsorption of micronutrients, decreased hemoglobin, or whether malnutrition increased psychomotor development delay susceptibility. Prospective cohort studies are needed to clarify this question and the mechanisms responsible. In addition, follow-up of children in primary care in terms of Giardia, diagnosis and treatment will have a positive effect on child health during the programme of growth monitoring. References 1. Fernandez ID, Himes JH, Onis de M. Prevalence of nutritional wasting in populations: building explanatory models using secondary data. Bull WHO 2002; 80: 282–91.
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Hosmer–Lemeshow (p = 0.748).
2. Cross AW. Maternal and child health. In: Wallace RB (eds.), Maxcy-Rosenau-Last Public Health and Preventive Medicine, 14th edn. Appleton and Lange, Stanford Connecticut, 1998; 1173–75. 3. Thompson RCA, Reynoldson JA. Giardia and giardiasis. Adv Parasitol 1993; 32: 71–160. 4. Lengerich EJ, Addiss DG, Juranek DD. Severe giardiasis in the United States. Clin Infect Dis 1994; 18: 760–63. 5. Loewenson R, Mason PR, Patterson BA. Giardiasis and the nutritional status of Zimbabwean schoolchildren. Ann Trop Paediatr 1986; 6: 73–8. 6. Solomons NW. Giardiasis: nutritional implications. Rev Infect Dis 1982; 4: 859–69. 7. Sackey ME, Weigel MM, Armijos RX. Predictors and nutritional consequences of intestinal parasitic infections in rural Ecuadorian children. J Trop Pediatr 2003; 49: 17–23. 8. Stephenson LS, Latham MC, Ottesen EA. Malnutrition and parasitic helmints infections. Parasitology 2000; 121: 23–38. 9. Oberhelman RA, Guerrero ES, Fernandez ML, et al. Correlations between intestinal parasitosis, physical growth, and psychomotor development among infants and children from rural Nicaragua. Am J Trop Med Hyg 1998; 58: 470–75. 10. Farthing MJG. New perspectives in giardiasis. J Med Microbiol 1992; 37: 1–2. 11. Erol N, Sezgin N, Savașir I. Gelișim Tarama Envanteri ile ilgili gecerlik calismalari. Türk Psikoloji Dergisi 1993; 8: 16. 12. Savașir I, Sezgin N, Erol N. 0–6 yaș cocukları icin Gelișim Tarama Envanteri Geliștirilmesi: Ön calıșmalar. Türk Psikiyatri Dergisi 1992; 3: 33. 13. Savașir I, Sezgin N, Erol N. Ankara Gelișim Tarama Envanteri El Kitabı (2nd edn). Rekmay, Ankara, 1998. 14. Dibley MJ, Goldsby JB, Staehling NW, Trowbridge FL. Development of normalized curves for the international growth reference: historical and technical considerations. Am J Clin Nutr 1987; 46: 736–48. 15. Al-Shammari, Kyoja T, El-khwasky, Gad A. Intestinal parasitic diseases in Riyadh, Saudi Arabia: prevalance, sociodemographic and environmental associates. Trop Med Int Health 2001; 6: 184–89. 16. Heresi G. Giardia. Pediatr Rev 1997; 18: 243–47. 17. Özcelik S, Deg˘erli S. Giardiosis. Acta Parasitol Turcica 1998; 22: 292–98. 18. Wilson ME. Giardiasis. In: Wallace RB (ed.), Maxcy-RosenauLast Public Health and Preventive Medicine, 14th edn. Appleton & Lange, Stanford, Connecticut, 1998; 252–54. 19. Lunn PG, Hezekioh EO, Northrop-Clewes CA, Boyce SA. Giardia intestinalis is unlikely to be a major cause of poor growth of rural Gambian infants. J Nutr 1998; 129: 872–77. 20. Saldiva SR, Silveira AS, Philippi ST, et al. Ascaris trichuris association and malnutrition in Brazilian children. Pediatr Perinat Epidem 1999; 13: 89–98.
