Pesticide Exposure and Stunting among Children in Agricultural Areas

Apoina Kartin1, Hertanto Wahyu Subagio2, Suharyo Hadisaputro3,4, Martha Irene Kartasurya1, Suhartono Suhartono5, Budiyono Budiyono5
1Department of Public Health Nutrition, Fac-ulty of Public Health, Diponegoro University, Semarang, Indonesia
2Department of Nutrition, Faculty of Medicine, Diponegoro University, Semarang, Indonesia
3Department of Internal Medicine
4Department of Internal Medicine, Faculty of Medicine, Diponegoro University, Semarang, Indonesia
5Department of Envi-ronmental Health, Fac-ulty of Public Health, Diponegoro University, Semarang, Indonesia

Tóm tắt

Background: The prevalence of growth disorders among school-aged children in Indonesia is high (30.7%). Pesticides have been massively used in Indonesian agricultural areas. Objective: To determine if exposure to pesticides is associated with stunting among children in agricultural areas. Methods: This case-control study included 160 children (48 cases and 112 controls) aged 8–12 years. Exposure to pesticides was measured based on the history of the exposure since perinatal period, infancy, and childhood of the participants. Stunting was determined as a height for age z-score (HAZ) < -2 SD. Other variables measured were levels of thyroid stimulating hormone (TSH), insulin-like growth factor-1 (IGF-1), hemoglobin, zinc, albumin, nutrient adequacy level (energy and protein), and history of infection, low-birth weight (LBW), and mother's height. Results: There were no significant difference between the cases and controls in terms of in the baseline characteristics, except for the median IGF-1 level; it was significantly (p<0.001) lower in the cases (66.73 ng/mL) than the controls (112.57 ng/mL). High level of pesticide exposure (p=0.029) and low IGF-1 levels (p<0.001) were significantly associated with stunting. After adjusting for confounding variables, these variables were found to be independent risk factors for stunting in children (aOR 3.90, 95% CI 1.15 to 13.26; and aOR 8.35, 95% CI 3.65 to 19.14, respectively). Conclusion: Pesticide exposure could be a risk factor for the occurrence of growth disorders in children living in agricultural areas. Necessary actions should be taken to protect children living in agricultural areas from exposure to pesticides.

Từ khóa


Tài liệu tham khảo

Gibson R. Principles of Nutritional Assessment. 2nd ed. New York, Oxford University Press, Inc, 2005.

Mikhail W, 2013, Effect of Nutritional Status on Growth Pattern of Stunted Preschool Children in Egypt National Nutrition Institute (NNI), Cairo, Egypt, Acad J Nutr, 2, 1

Nicol L, Allen D, Czernichow P, Zeitler P. Normal growth and growth disorders. In: Kappy M, Allen D, Geffner M, eds. Pediatric Practice Endocrinology. New York, The McGraw-Hill Companies, Inc, 2010:23-79.

Candra A, 2011, Risk factors of stunting among 1-2 years old children in Semarang City, Media Medica Indonesa, 45, 206

Paudel R, 2012, Risk Factors for Stunting Among Children: A Community Based Case Control Study in Nepal, Kathmandu Univ Med J, 39, 18

Vogiatzi M, 1998, The Short Child, Pediatrics in Review, 19, 92, 10.1542/pir.19-3-92

Kar B, 2008, Cognitive development in children with chronic protein energy malnutrition, Behav Brain Funct, 4, 31, 10.1186/1744-9081-4-31

Sokolovic N, 2014, Catch-up growth does not associate with cognitive development in Indian school-age children, Eur J Clin Nutr, 68, 14, 10.1038/ejcn.2013.208

Brito G, 2006, Growth status and academic performance in Brazilian school age children: growth retardation impairs mathematical, but not reading and spelling abilities TT - Crescimento e desempenho acadêmico em escolares brasileiros: retardo no crescimento interfere co, Arq Neuropsiquiatr, 64, 921, 10.1590/S0004-282X2006000600006

Prendergast A, 2014, The stunting syndrome in developing countries, Paediatr Int Child Health, 34, 250, 10.1179/2046905514Y.0000000158

Indonesian Health Ministry. National Survey on Primary Health Report. 2013.

Suhartono S, 2018, Pesticide exposure and thyroid function in elementary school children living in an agricultural area, Brebes district, Indonesia, Int J Occup Environ Med, 9, 137, 10.15171/ijoem.2018.1207

Boada L, 2007, Serum levels of insulin-like growth factor-I in relation to organochlorine pesticides exposure, Growth Horm IGF Res, 17, 506, 10.1016/j.ghir.2007.05.004

Zumbado M, 2010, Insulin-like growth factor-I (IGF-I) serum concentrations in healthy children and adolescents: Relationship to level of contamination by DDT-derivative pesticides, Growth Horm IGF Res, 20, 63, 10.1016/j.ghir.2009.07.003

Idohou-Dossou N, 2003, Nutritional status of preschool Senegalese children: long-term effects of early severe malnutrition, Br J Nutr, 90, 1123, 10.1079/BJN2003990

Rauh V, 2006, Impact of Prenatal Chlorpyrifos Exposure on Neurodevelopment in the First 3 Years of Life Among Inner-City Children, Pediatrics, 118, e1845, 10.1542/peds.2006-0338

Bouchard M, 2010, Attention-deficit/hyperactivity disorder and urinary metabolites of organophosphate pesticides, Pediatrics, 125, e1270, 10.1542/peds.2009-3058

Budiyono, 2015, Pesticide Metabolites, Anti-Thyroid Peroxidase and Thyroid Stimulating Hormone Status in School Children: A Preliminary Study in Agriculture Areas in Indonesia, Int J Sci Basic Appl Res, 22, 1

Kartini A, 2018, Goiter and hypothyroidism among elementary school children in lowland agricultural area, Brebes District Indonesia, Indian J Public Heal Res Dev, 9, 120, 10.5958/0976-5506.2018.00980.4

Diamanti-Kandarakis E, 2009, Endocrine-Disrupting Chemicals: An Endocrine Society Scientific Statement, Endocr Rev, 30, 293, 10.1210/er.2009-0002

Stone MB, Wallace RB. Medicare Coverage of Routine Screening for Thyroid Dysfunction. Washington DC, The National Academic Press, 2003.

Lemeshow S, Hosmer Jr D, Klar J, Lwanga S. Adequacy of Sample Size in Health Studies. New York, John Wiley & Sons Ltd, 1993.

World Health Organization. WHO Child Growth Standards. Geneva: WHO Press, 2006.

Schlesselman J, Stolley P. Case-Control Studies. Design, Conduct, Analysis. New York, Oxford University Press, 1982.

Youden W, 1950, Index for rating diagnostic tests, Cancer, 3, 32, 10.1002/1097-0142(1950)3:1<32::AID-CNCR2820030106>3.0.CO;2-3

Habibzadeh F, 2016, On determining the most appropriate test cut-off value: the case of tests with continuous results, Biochem Medica, 26, 297, 10.11613/BM.2016.034

World Health Organization, 2011, Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity, 1

Dehghani S, 2011, Prevalence of Zinc Deficiency in 3-18 Years Old Children in Shiraz-Iran, Iran Red Crescent Med J, 13, 4

Abdullah SF, 2014, Serum Albumin Level in Sudanese Children with Edematous and Non-Edematous Malnutrition, Asian Journal of Biomedical and Pharmaceutical Sciences, 4, 47

Yasmin G, 2014, Risk factors of stunting among school-aged children from eight provinces in Indonesia, Pak J Nutr, 13, 557, 10.3923/pjn.2014.557.566

World Health Organization, 1996, Catalogue of health indicators, 37

de Onis M, 2016, Childhood stunting: a global perspective, Matern Child Nutr, 12, 12, 10.1111/mcn.12231

Umeta M, 2003, Factors Associated with Stunting in Infants Aged 5 – 11 Months in the Dodota-Sire District , Rural Ethiopia, J Nutr, 133, 1064, 10.1093/jn/133.4.1064

Esfivariz C, 1997, Nutrition and the Insulin-Like Growth Factor System, Endocrine, 7, 65, 10.1007/BF02778066

Skottner A, 2012, Biosynthesis of Growth Hormone and Insulin-Like Growth Factor-I and the Regulation of their Secretion, Open Endocrinol J, 6, M2), 10.2174/1874216501206010003

Gibson R, 2007, Does zinc deficiency play a role in stunting among primary school children in NE Thailand?, British Journal of Nutrition, 97, 167, 10.1017/S0007114507250445

Ninh N, 1995, Reduced liver insulin-like growth factor-I gene expression in young zinc-deprived rats is associated with a decrease in liver growth hormone (GH) receptors and serum GH-binding protein, J Endocrinol, 144, 449, 10.1677/joe.0.1440449

Yamaguchi M, 2007, Role of zinc in bone metabolism and preventive effect on bone disorder, Biomed Res Trace Elem, 18, 346

Salgueiro M, 2002, The Role of Zinc in the Growth and Development of Children, Nutrition, 18, 510, 10.1016/S0899-9007(01)00812-7

Rivera M, 2003, Trace elements, innate immune response and parsites pdf, Clin Chem Lab Med, 41, 1020, 10.1515/CCLM.2003.156

Watanabe M, 2010, Protein Intakes and Serum Albumin Levels in a Japanese General Population: NIPPON DATA90, J Epidemiol 2010, 20, S531

Crane R, 2015, Environmental enteric dysfunction: An overview, Food Nutr Bull, 36, S76, 10.1177/15648265150361S113

Miller G, 2014, The Nature of Nurture : Refining the Definition of the Exposome, Toxicol Sci, 137, 1, 10.1093/toxsci/kft251

Lin A, 2013, Household Environmental Conditions Are Associated with Enteropathy and Impaired Growth in Rural Bangladesh, Am J Trop Med Hyg, 89, 130, 10.4269/ajtmh.12-0629

Prendergast A, 2012, Review : Enteropathies in the Developing World: Neglected Effects on Global Health, Am J Trop Med Hyg, 86, 756, 10.4269/ajtmh.2012.11-0743

Mapesa J, 2016, An Exposome Perspective on Environmental Enteric Dysfunction, Environ Health Perspect, 124, 1121, 10.1289/ehp.1510459

Owino V, 2016, Environmental Enteric Dysfunction and Growth Failure / Stunting in Global Child Health, Pediatrics, 138, 1, 10.1542/peds.2016-0641

Prendergast AJ, 2014, Stunting is characterized by chronic inflammation in Zimbabwean infants, PLoS One, 9, e86928, 10.1371/journal.pone.0086928

Lukaszewicz-hussain A, 2010, Role of oxidative stress in organophosphate insecticide toxicity – Short review, Pestic Biochem Physiol, 98, 145, 10.1016/j.pestbp.2010.07.006

Degen A. Effect of macroparasites on the energy budget of small mammals. In: Morand S, Krasnov Y, Poulin R, eds. In: Morand S, Krasnov Y, Poulin R, eds. Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo, Springer-Verlag, 2006:371-400.

Weiner J, 1992, Physiological limits to Energy Budgets Sustainable in Birds and Mammals: Ecological Implications, Trends Ecol Evol, 7, 384, 10.1016/0169-5347(92)90009-Z

Narváez C, 2016, Subchronic exposure to chlorpyrifos affects energy expenditure and detoxification capacity in juvenile Japanese quails, Chemosphere, 144, 775, 10.1016/j.chemosphere.2015.09.060

Xu Y, 2014, Correlation between serum IGF-1 and blood lead level in short stature children and adolescent with growth hormone deficiency, Int J Clin Exp Med, 7, 856

Goldner W, 2010, Pesticide use and thyroid disease among women in the agricultural health study, Am J Epidemiol, 171, 455, 10.1093/aje/kwp404

Farokhi F, 2014, Pesticide exposure and thyroid function in adult male sprayers, Int J Med Invest, 3, 127

Piccoli C, 2016, Pesticide exposure and thyroid function in an agricultural population in Brazil, Environ Res, 151, 389, 10.1016/j.envres.2016.08.011

Setian N, 2007, Hypothyroidism in children: diagnosis and treatment, J Pediatr (Rio J), 83, S209

Boas M, 2006, Environmental chemicals and thyroid function, Eur J Endocrinol, 154, 599, 10.1530/eje.1.02128

Wade M, 2002, Thyroid toxicity due to subchronic exposure to a complex mixture of 16 organochlorines, lead, and cadmium, Toxicol Sci, 67, 207, 10.1093/toxsci/67.2.207

Guntur A, 2013, IGF-1 regulation of key signaling pathways in bone, Bonekey Rep, 2, 1, 10.1038/bonekey.2013.171

Laron Z, 2001, Insulin-like growth factor 1 (IGF-1): a growth hormone, Mol Pathol, 54, 311, 10.1136/mp.54.5.311

Fleisch AF, 2013, Blood lead levels and serum insulin-like growth factor 1 concentrations in peripubertal boys, Environ Health Perspect, 121, 854, 10.1289/ehp.1206105

Boas M, 2010, Childhood exposure to phthalates: Associations with thyroid function, insulin-like growth factor I, and growth, Environ Health Perspect, 118, 1458, 10.1289/ehp.0901331

Liu J, Goyer R, Waalkes P. Toxic effects of metals. In: Shanahan J, Naglieri C, eds. Casarett and Doull's Toxicology: The Basic Science of Poisons. 7th ed. New York, The McGraw-Hill Companies, Inc, 2008:931-79.

Ejaredar M, 2015, Phthalate exposure and childrens neurodevelopment: A systematic review, Environ Res, 142, 51, 10.1016/j.envres.2015.06.014