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Effect of Agricultural Pesticide on Precocious Puberty in Urban Children

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Effect of Agricultural Pesticide on Precocious Puberty in Urban Children Vol. 63, No. 4, 146–150, 2020 Original article CEP https://doi.org/10.3345/cep.2019.00416 Effect of agricultural pesticide on precocious puberty in urban children: an exploratory study Junghwan Suh, MD, Han Saem Choi, MD, Ahreum Kwon, MD, Hyun Wook Chae, MD, Ho-Seong Kim, MD, PhD Department of Pediatrics, Severance Children’s Hospital, Endocrine Research Institute, Yonsei University College of Medicine, Seoul, Korea Background: The incidence of precocious puberty has incre­ Introduction ased throughout the 20th century. The association between precocious puberty and endocrine disrupting chemicals includ­ Advanced pubertal timing and increasing incidence of precoci­ ing agricultural pesticides has been a subject of global study, but ous puberty have been observed worldwide throughout the last human data are lacking. century. Previously, these trends were largely explained by im­ Purpose: We investigated the relationship between agricultural proved public health and nutrition, but endocrine disrupting pesticides and the development of precocious puberty. chemicals (EDCs) are recently drawing public scrutiny. EDCs Methods: We enrolled 60 female subjects at Severance Child­ are exogenous substances or mixtures that alter functions of the ren’s Hospital from December 2015 to January 2017. Of them, endocrine sys tem,1) including bisphenol A (BPA), phthalates, 30 were diagnosed with precocious puberty, while the other 30 heavy metals, agricultural pesticides, and pollutants such as dioxin prepubertal girls were enrolled as normal controls. We investi­ and polychlo rinated biphenyls, among others. Recent studies gated their clinical characteristics and analyzed the urinary levels have reported an association between EDCs and pubertal timing of 320 different agricultural pesticides. in humans and in animal models, but a conclusive relationship re­ Results: Agricultural pesticide was detected in one of 30 pati­ mains controversial. For example, BPA was once reported to have ents with precocious puberty (3.3%) versus 2 of 30 girls in the estrogenic effects causing precocious puberty in girls,2) but other normal control group (3.3% vs. 6.7%, P=0.554). Dinotefuran, a studies showed no direct relationship between urinary BPA level neonicotinoid­class insecticide, was detected in the samples of all and early puberty onset.3,4) Also, phthalates have been highlighted 3 positive subjects. as influencing precocious puberty, and have been widely inves­ Conclusion: Our results showed no relationship between tigated in humans and in animal models, but out comes from these agri cultural pesticides and the development of precocious pub­ studies are inconclusive.5­7) erty. Larger sample sizes and robustly controlled variables are Pesticides, which have been increasingly used in modern agri­ necessary to further investigate this topic. culture industry, have been investigated for agonistic or antago­ nistic effects on the endocrine system.8) Dichlorodiphenyltrichlo­ Key words: Endocrine disrupting chemicals, Agricultural pesti­ roethane and its metabolites have estrogenic effects on the cide, Precocious puberty endo crine system, causing precocious puberty.9) Methoxychlor and endosulfan were also reported to have estrogenic effects by directly binding to estrogen receptors, increasing estrogen sensiti­ Key message vity, or stimulating endogenous estrogen production through the Question: Does agricultural pesticide effect precocious puberty gonadotropin­releasing hormone (GnRH) system.10,11) Mean­ in girls? while, the fungicide prochloraz showed antiestrogenic effects in Dinotefuran, an insecticide of neonicotinoid class, was Finding: animal models,12) while exposure to organochlorine pesticides detected in one of 30 patients with precocious puberty, and in was associated with delayed pubertal development.13) In particul­ 2 girls of the normal control group, which was not statistically significant. ar, the matter of contaminated egg with insecticides attracted Meaning: There was no close relationship between agricultural intense public attention in Belgium and Korea in 2017. 14) pesticides and development of precocious puberty. However, there is an insufficient human subject data about the effects of pesticides, especially in Korean subjects. Therefore, we investigated the relationship between agricultural pesticides and development of precocious puberty. Corresponding author: Ho-Seong Kim, MD, PhD. Department of Pediatrics, Severance Children’s Hospital, Endocrine Research Institute, Yonsei University College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu, Seoul 03722, Korea E-mail: [email protected], ORCID: http://orcid.org/0000-0003-1135-099X Received: 3 May, 2019, Revised: 23 October, 2019, Accepted: 1 December, 2019 This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by- nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Copyright © 2020 by The Korean Pediatric Society Methods and were vortexed for 1 minute at maximum speed. After the reaction was complete, the tubes were centrifuged at 4,500 rpm 1. Study participants for 5 minutes. Next, 1 mL of supernatant was transferred to a We enrolled 60 female subjects at Severance Children’s Hospi­ dispersive SPE tube containing 25­mg primary­secondary amine, tal from December 2015 to January 2017. Thirty patients were and 150­mg MgSO4 and mixed for 1 minute. Finally, the tube diagnosed with precocious puberty based on peak luteinizing was centrifuged at 12,000 rpm for 5 minutes and the supernatant hormone (LH) level over 5 mIU/mL on a GnRH stimulation test, was filtered through a 0.2­μm syringe filter. and 30 prepubertal girls were classified into the normal control group. We analyzed patient anthropometric data, laboratory 4. Preparation of standard pesticide solutions and reagents results, and bone age, and we sent blood and urine samples to the Standard pesticide solutions were purchased from Ultra Korea Agriculture Food Analysis Institute for analysis of agricul­ Scientific (North Kingston, RI, USA). Triphenylphosphate, tural pesticides. A total of 320 kinds of agricultural pesticides, which was used as an internal standard was purchased from including dichlorodiphenyldichlorethylene (DDE) (geome tric Sigma­Aldrich (St. Louis, MO, USA). Pesticide grade acetonitrile mean 1.45 ng/g) and hexachlorobenzene (geometric mean 0.092 (MeCN) was purchased from Duksan (Seoul, Korea). The ng/g), were analyzed by liquid chromatography mass spectro­ GCMS­TQ8050 (GC­MS/MS) and LCMS­TQ8050 (LC­MS/ metry (LC­MS/MS) and gas chromatography mass spectrometry MS) analytical instruments were from Shimadzu (Kyoto, Japan). (GC­MS/MS) (Supplementary material 1). The present study protocol was reviewed and approved by the Institutional Re­ 5. LC-MS/MS condition view Board of Yonsei University Health System in Seoul, Korea LC­MS/MS analysis was performed to detect pesticide com­ (approval number: 4­2019­0040). Informed consent was sub­ ponents in the urine samples,18) using the following conditions; mitted by all subjects when they were enrolled. a Capcell Core C18 column (2.1 mm×150 mm, 2.7 μm), 3­μL injection volume, and 40°C column temperature. Ionization was 2. Biochemical and clinical assessment performed by electrospray ionization (polarity, positive). Two Baseline characteristics of age, height, weight, body mass in­ mobile phases were used; mobile A contained 0.1% formic acid dex (BMI), LH, follicle­stimulating hormone (FSH), estradiol, and 5 mM ammonium formate in water; mobile B contained and bone age were examined during each patient’ first clinic 0.1% formic acid and 5 mM ammonium formate in methanol. visit. LH and FSH serum levels were estimated using sequential The flow rate was 0.3 mL per minute. Flow rates and times are 2­step immunoenzymatic assay (Access hLH, FSH Reagent Pack; shown in Supplementary material 2. Beckman Coulter Inc., La Brea, CA, USA) with an intra­assay coefficient of variation (CV) of 3.5%–5.4%, an interassay CV of 6. GC-MS/MS condition 4.3%–6.4%, and a lower limit of detection of 0.2 IU/L for both The GCMS­TQ8050 instrument from Shimadzu (Kyoto, gonadotropins. Serum estradiol level was measured via radio­ Japan) was used with the Rxi­5MS capillary column (length, 20 immunoassay (Coat­A­Count Estradiol; Siemens, Erlangen, mm; inner diameter, 0.18 mm; film thickness, 0.18 μm; Restek, Germany) with an intra­assay CV of 4.0%–7.0%, an interassay Bellefonte, PA, USA) for gas chromatography mass spectrometry. CV of 4.2%–8.1%, and a lower limit of detection of 8 pg/mL. The inlet temperature was 260°C, and the column flow rate Bone age was determined using the Greulich­Pyle method with was 1 mL per minute. The injection volume was 1 μL, and the radiography on the left hand and wrist. Height standard deviation splitless mode was used. During GCMS­TQ8050 analysis, the score (SDS), weight SDS, and BMI SDS were calculated from the interface temperature was maintained at 250°C. 2017 Korean children and adolescents’ growth standard.15) 7. Statistical analyses 3. Urine sample preparations Statistical analyses were performed using IBM SPSS ver. 23.0 Urine samples were collected into 50­mL Falcon tube (BD Bio­ (IBM Co., Armonk, NY, USA). Two­sample t test was used to sciences, San Jose, CA, USA) in the early morning and stored at compare baseline characteristics between the 2 groups, and the ­20°C until pesticide
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