Abstract
The present study aims to evaluate the effects of pesticides on premature breast development. Forty-five girls (group 1) with premature breast development living in the Menderes region, where greenhouse cultivation is the main income, 16 girls (group 2) living in Izmir city with early puberty, and 33 girls (group 3) who had no signs of puberty were included in the study. Endosulphan 1, endosulphan 2, endosulphan sulphate, methoxychlor, vinclozolin, 4,4-dichlorodiphenyldichlorethylene (DDE), 4,-dichlorodiphenyltrichloroethane (DDT), and 2,4-DDT were evaluated in the serum and adipose tissues of the groups by using a gas chromatography–mass spectrometry method. With the exception of 4,4′-DDE, the pesticides studied were undetectable in the serum and adipose tissue samples. The levels of basal luteinizing hormone (LH), stimulated LH, follicle-stimulating hormone, and the long axis of the uterus and both ovaries were significantly different in the girls who had premature thelarche and detectable 4,4′-DDE levels compared to the girls who had premature thelarche and undetectable 4,4′-DDE levels in serum and adipose tissues. The presence and levels of pesticides in serum and adipose tissues were not related to precocious puberty (PP). The mechanisms that lead to PP may also result in obesity, and obesity may be the underlying cause for PP in this group.
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Abaci, A., Demir, K., Bober, E., & Buyukgebiz, A. (2009). Endocrine disrupters—with special emphasis on sexual development. Pediatric Endocrinology Reviews, 6, 464–475.
Anderson, S. E., & Must, A. (2005). Interpreting the continued decline in the average age at menarche: results from two nationally representative surveys of U.S. girls studied 10 years apart. The Journal of Pediatrics, 147, 753–760.
Badouraki, M., Christoforidis, A., Economou, I., Dimitriadis, A. S., & Katzos, G. (2008). Evaluation of pelvic ultrasonography in the diagnosis and differentiation of various forms of sexual precocity in girls. Ultrasound in Obstetrics & Gynecology, 32, 819–827.
Blanck, H. M., Marcus, M., Hertzberg, V., Tolbert, P. E., Rubin, C., Henderson, A. K., et al. (2000). Determinants of polybrominated biphenyl serum decay among women in the Michigan PBB cohort. Environmental Health Perspectives, 108, 147–152.
Blanck, H. M., Marcus, M., Tolbert, P. E., Rubin, C., Henderson, A. K., Hertzberg, V. S., et al. (2000). Age at menarche and tanner stage in girls exposed in utero and postnatally to polybrominated biphenyl. Epidemiology, 11, 641–647.
Blystone, C. R., Lambright, C. S., Cardon, M. C., Furr, J., Rider, C. V., Hartig, P. C., et al. (2009). Cumulative and antagonistic effects of a mixture of the antiandrogens vinclozolin and iprodione in the pubertal male rat. Toxicological Sciences, 111, 179–188.
Buck Louis, G. M., Gray, L. E., Jr., Marcus, M., Ojeda, S. R., Pescovitz, O. H., Witchel, S. F., et al. (2008). Environmental factors and puberty timing: expert panel research needs. Pediatrics, 121, S192–S207.
Carel, J. C., & Léger, J. (2008). Clinical practice. Precocious puberty. The New England Journal of Medicine, 358, 2366–2377.
Cavallo, A., & Zhou, X. H. (1994). LHRH test in the assessment of puberty in normal children. Hormone Research, 41, 10–15.
Cavallo, A., Richards, G. E., Busey, S., & Michaels, S. E. (1995). A simplified gonadotrophin-releasing hormone test for precocious puberty. Clinical Endocrinology (Oxf), 42, 641–646.
Codner, E., & Román, R. (2008). Premature thelarche from phenotype to genotype. Pediatric Endocrinology Reviews, 5, 760–765.
Cok, I., Bilgili, A., Yarsan, E., Bagci, C., & Burgaz, S. (1998). Organochlorine pesticide residue levels in human adipose tissue of residents of Manisa (Turkey), 1995–1996. Bulletin of Environmental Contamination and Toxicology, 61, 311–316.
Colón, I., Caro, D., Bourdony, C. J., & Rosario, O. (2000). Identification of phthalate esters in the serum of young Puerto Rican girls with premature breast development. Environmental Health Perspectives, 108, 895–900.
Cooper, R. L., & Kavlock, R. J. (1997). Endocrine disruptors and reproductive development: a weight-of-evidence overview. The Journal of Endocrinology, 152, 159–166.
Dattani, M., & Hindmarsh, P. (2005). Normal and abnormal puberty. In C. Brook, P. Clayton, & R. Brown (Eds.), Brook’s clinical pediatric endocrinology (pp. 182–210). Massachusetts: Blackwell Publishing.
de Vries, L., Horev, G., Schwartz, M., & Phillip, M. (2006). Ultrasonographic and clinical parameters for early differentiation between precocious puberty and premature thelarche. European Journal of Endocrinology, 154, 891–898.
Den Hond, E., & Schoeters, G. (2006). Endocrine disrupters and human puberty. International Journal of Andrology, 29, 264–290.
Denham, M., Schell, L. M., Deane, G., Gallo, M. V., Ravenscroft, J., DeCaprio, A. P., et al. (2005). Relationship of lead, mercury, mirex, dichlorodiphenyldichloroethylene, hexachlorobenzene, and polychlorinated biphenyls to timing of menarche among Akwesasne Mohawk girls. Pediatrics, 115, e127–e134.
Diamanti-Kandarakis, E., Bourguignon, J. P., Giudice, L. C., Hauser, R., Prins, G. S., Soto, A. M., et al. (2009). Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocrine Reviews, 30, 293–342.
Fenton, S. E. (2006). Endocrine-disrupting compounds and mammary gland development: early exposure and later life consequences. Endocrinology, 147, S18–S24.
Gladen, B. C., Ragan, N. B., & Rogan, W. J. (2000). Pubertal growth and development and prenatal and lactational exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene. The Journal of Pediatrics, 136, 490–496.
Golub, M. S., Hogrefe, C. E., Germann, S. L., Lasley, B. L., Natarajan, K., & Tarantal, A. F. (2003). Effects of exogenous estrogenic agents on pubertal growth and reproductive system maturation in female rhesus monkeys. Toxicological Sciences, 74, 103–113.
Gray, L. E., Jr., Ostby, J., Ferrell, J., Rehnberg, G., Linder, R., Cooper, R., et al. (1989). A dose-response analysis of methoxychlor-induced alterations of reproductive development and function in the rat. Fundamental and Applied Toxicology, 12, 92–108.
Guo, Y. L., Lambert, G. H., Hsu, C. C., & Hsu, M. M. (2004). Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans. International Archives of Occupational and Environmental Health, 77, 153–158.
Herman-Giddens, M. E. (2007). Puberty is starting earlier in the 21st century. In O. H. Pescovitz & E. C. Walvoord (Eds.), When puberty is precocious: scientific and clinical aspects (pp. 105–136). Totowa: Humana Press.
Herter, L. D., Golendziner, E., Flores, J. A., Moretto, M., Di Domenico, K., Becker, E., Jr., et al. (2002). Ovarian and uterine findings in pelvic sonography: comparison between prepubertal girls, girls with isolated thelarche, and girls with central precocious puberty. Journal of Ultrasound in Medicine, 21, 1237–1246.
Ikegami, S., Moriwake, T., Tanaka, H., Inoue, M., Kubo, T., Suzuki, S., et al. (2001). An ultrasensitive assay revealed age-related changes in serum oestradiol at low concentrations in both sexes from infancy to puberty. Clinical Endocrinology (Oxf), 55, 789–795.
Jacobson-Dickman, E., & Lee, M. M. (2009). The influence of endocrine disruptors on pubertal timing. Current Opinion in Endocrinology, Diabetes, and Obesity, 16, 25–30.
Kaplowitz, P. (2007). BMI and onset of puberty. In O. H. Pescovitz & E. C. Walvoord (Eds.), When puberty is precocious: scientific and clinical aspects (p. 137). New Jersey: Humana Press.
Kaplowitz, P. B., Slora, E. J., Wasserman, R. C., Pedlow, S. E., & Herman-Giddens, M. E. (2001). Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics, 108, 347–353.
Karlberg, J. (2002). Secular trends in pubertal development. Hormone Research, 57, 19–30.
Khurana, S., Ranmal, S., & Ben-Jonathan, N. (2000). Exposure of newborn male and female rats to environmental estrogens: delayed and sustained hyperprolactinemia and alterations in estrogen receptor expression. Endocrinology, 141, 4512–4517.
Klein, K. O., Mericq, V., Brown-Dawson, J. M., Larmore, K. A., Cabezas, P., & Cortinez, A. (1999). Estrogen levels in girls with premature thelarche compared with normal prepubertal girls as determined by an ultrasensitive recombinant cell bioassay. The Journal of Pediatrics, 134, 190–192.
Krstevska-Konstantinova, M., Charlier, C., Craen, M., Du Caju, M., Heinrichs, C., de Beaufort, C., et al. (2001). Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides. Human Reproduction, 16, 1020–1026.
Lee, P. A., & Houk, C. P. (2007). Puberty and its disorders. In F. Lifshitz (Ed.), Pediatric endocrinology (pp. 273–303). New York: Informa Healthcare.
Markey, C. M., Luque, E. H., Munoz De Toro, M., Sonnenschein, C., & Soto, A. M. (2001). In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biology of Reproduction, 65, 1215–1223.
Marshall, W. A., & Tanner, J. M. (1969). Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood, 44, 291–303.
Marty, M. S., Crissman, J. W., & Carney, E. W. (1999). Evaluation of the EDSTAC female pubertal assay in CD rats using 17beta-estradiol, steroid biosynthesis inhibitors, and a thyroid inhibitor. Toxicological Sciences, 52, 269–277.
Massart, F., Parrino, R., Seppia, P., Federico, G., & Saggese, G. (2006). How do environmental estrogen disruptors induce precocious puberty? Minerva Pediatrica, 58, 247–254.
Masutomi, N., Shibutani, M., Takagi, H., Uneyama, C., Takahashi, N., & Hirose, M. (2003). Impact of dietary exposure to methoxychlor, genistein, or diisononyl phthalate during the perinatal period on the development of the rat endocrine/reproductive systems in later life. Toxicology, 192, 149–170.
McLachlan, J. A., Simpson, E., & Martin, M. (2006). Endocrine disrupters and female reproductive health. Best Practice & Research. Clinical Endocrinology & Metabolism, 20, 63–75.
Mul, D., Oostdijk, W., & Drop, S. L. (2002). Early puberty in adopted children. Hormone Research, 57, 1–9.
Muñoz-de-Toro, M., Markey, C. M., Wadia, P. R., Luque, E. H., Rubin, B. S., Sonnenschein, C., et al. (2005). Perinatal exposure to bisphenol-A alters peripubertal mammary gland development in mice. Endocrinology, 146, 4138–4147.
Nebesio, T. D., & Pescovitz, O. H. (2007). The role of endocrine disruptors in pubertal development. In O. H. Pescovitz & E. C. Walvoord (Eds.), When puberty is precocious: scientific and clinical aspects (pp. 425–419). New Jersey: Humana Press.
Neely, E. K., Wilson, D. M., Lee, P. A., Stene, M., & Hintz, R. L. (1995). Spontaneous serum gonadotropin concentrations in the evaluation of precocious puberty. The Journal of Pediatrics, 127, 47–52.
Neyzi, O., Binyıldız, P., & Alp, H. (1978). Türk çocuklarında büyüme-gelişme normları. I. Tartı ve boy değerleri. Ýstanbul Týp Fakültesi Mecmuasý, 41, 74–81.
Ouyang, F., Perry, M. J., Venners, S. A., Chen, C., Wang, B., Yang, F., et al. (2005). Serum DDT, age at menarche, and abnormal menstrual cycle length. Occupational and Environmental Medicine, 62, 878–884.
Parent, A. S., Teilmann, G., Juul, A., Skakkebaek, N. E., Toppari, J., & Bourguignon, J. P. (2003). The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocrine Reviews, 24, 668–693.
Pitarch, E., López, F. J., Serrano, R., & Hernández, F. (2001). Multiresidue determination of organophosphorus and organochlorine pesticides in human biological fluids by capillary gas chromatography. Fresenius’ Journal of Analytical Chemistry, 369, 502–509.
Presibella, K. M., Kita, D. H., Carneiro, C. B., Andrade, A. J., & Dalsenter, P. R. (2005). Reproductive evaluation of two pesticides combined (deltamethrin and endosulfan) in female rats. Reproductive Toxicology, 20, 95–101.
Resende, E. A., Lara, B. H., Reis, J. D., Ferreira, B. P., Pereira, G. A., & Borges, M. F. (2007). Assessment of basal and gonadotropin-releasing hormone-stimulated gonadotropins by immunochemiluminometric and immunofluorometric assays in normal children. The Journal of Clinical Endocrinology and Metabolism, 92, 1424–1429.
Rosenfield, R. L., Cooke, D. W., & Radovic, S. (2008). Puberty and its disorders in the female. In M. A. Sperling (Ed.), Pediatric endocrinology (pp. 530–609). Philadelphia: Saunders Elsevier.
Rosenfield, R. L., Lipton, R. B., & Drum, M. L. (2009). Thelarche, pubarche, and menarche attainment in children with normal and elevated body mass index. Pediatrics, 123, 84–88.
Roy, J. R., Chakraborty, S., & Chakraborty, T. R. (2009). Estrogen-like endocrine disrupting chemicals affecting puberty in humans—a review. Medical Science Monitor, 15, RA137–RA145.
Sagiv, S. K., Tolbert, P. E., Altshul, L. M., & Korrick, S. A. (2007). Organochlorine exposures during pregnancy and infant size at birth. Epidemiology, 18, 120–129.
Schoeters, G., Den Hond, E., Dhooge, W., van Larebeke, N., & Leijs, M. (2008). Endocrine disruptors and abnormalities of pubertal development. Basic & Clinical Pharmacology & Toxicology, 102, 168–175.
Stanhope, R. (2000). Premature thelarche: clinical follow-up and indication for treatment. Journal of Pediatric Endocrinology & Metabolism, 13, 827–830.
Sun, S. S., Schubert, C. M., Chumlea, W. C., Roche, A. F., Kulin, H. E., Lee, P. A., et al. (2002). National estimates of the timing of sexual maturation and racial differences among US children. Pediatrics, 110, 911–919.
Teilmann, G., Pedersen, C. B., Jensen, T. K., Skakkebaek, N. E., & Juul, A. (2005). Prevalence and incidence of precocious pubertal development in Denmark: an epidemiologic study based on national registries. Pediatrics, 116, 1323–1328.
Teilmann, G., Pedersen, C. B., Skakkebaek, N. E., & Jensen, T. K. (2006). Increased risk of precocious puberty in internationally adopted children in Denmark. Pediatrics, 118, e391–e399.
Varayoud, J., Monje, L., Bernhardt, T., Muñoz-de-Toro, M., Luque, E. H., & Ramos, J. G. (2008). Endosulfan modulates estrogen-dependent genes like a non-uterotrophic dose of 17beta-estradiol. Reproductive Toxicology, 26, 138–145.
Vasiliu, O., Muttineni, J., & Karmaus, W. (2004). In utero exposure to organochlorines and age at menarche. Human Reproduction, 19, 1506–1512.
Wohlfahrt-Veje, C., Andersen, H. R., Jensen, T. K., Grandjean, P., Skakkebæk, N. E., & Main, K. M. (2009). Long-term effects of prenatal pesticide exposure on several endocrine functions in children. Hormone Research, 72, 428–429.
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This study was supported by the Ege University Research Committee.
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Ozen, S., Darcan, S., Bayindir, P. et al. Effects of pesticides used in agriculture on the development of precocious puberty. Environ Monit Assess 184, 4223–4232 (2012). https://doi.org/10.1007/s10661-011-2257-6
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DOI: https://doi.org/10.1007/s10661-011-2257-6