Elsevier

Reproductive Toxicology

Volume 67, January 2017, Pages 174-185
Reproductive Toxicology

Occupational exposure to pesticides, reproductive hormone levels and sperm quality in young Brazilian men

https://doi.org/10.1016/j.reprotox.2017.01.001Get rights and content

Highlights

  • Lifetime pesticide use was associated with reduced LH and prolactin levels.

  • Lifetime use of pesticides was also associated with poorer sperm morphology.

  • Maternal farming during pregnancy was associated with larger AGD and TV.

  • Results support the hypothesis that pesticides may affect male reproductive system.

Abstract

The association of occupational exposure to current-use pesticides with reproductive hormones, semen quality, and genital measures was investigated among young men in the South of Brazil. A cross-sectional study was conducted in 99 rural and 36 urban men aged 18–23 years. Information on pesticide use was obtained through questionnaire. Serum and semen samples were analyzed for sex hormones and sperm parameters, respectively, and measurement of anogenital distance (AGD) and testis volume (TV) were performed. Associations were explored using multivariate linear regression. Rural men had poorer sperm morphology, higher sperm count, and lower LH levels relative to urban subjects. Lifetime use of pesticides, especially herbicides and fungicides, was associated with poorer morphology and reduced LH and prolactin, with evidence of a linear pattern. Maternal farming during pregnancy was associated with larger AGD and TV. Chronic occupational exposure to modern pesticides may affect reproductive outcomes in young men.

Introduction

Endocrine disrupting chemicals (EDCs) are compounds that alter the normal functioning of the endocrine system of both wildlife and humans [1]. Increasing human exposure to EDCs has been hypothesized to play a causative role in some of the observed adverse trends in male reproductive health, such as undescended testes, hypospadias, decreased sperm quality, and testicular cancer [2].

Many modern pesticides possess hormonal activity and have thus been classified as EDCs. In vitro studies of a variety of non-persistent pesticides suggest that they may exert estrogenic and anti-androgenic activity and disturb sex steroid-synthesizing enzymes [3], [4]. Given their endocrine-disrupting potential, several epidemiological studies have explored the association between exposure to currently-used pesticides and altered sperm quality [5], [6], [7], [8]. Most data are from occupational studies linking exposure to moderate-high levels of multiple pesticides and poor semen quality, based on decreased concentration and motility, low percentage of morphologically normal spermatozoa, and changes in sperm DNA [6], [9]. Because pesticides are a heterogeneous group of substances with diverse chemical structures and mechanisms of action, some pesticides may directly affect spermatogenesis by damaging or destroying Sertoli cells and other spermatogenesis support cells, whereas others may act indirectly by altering hormonal signaling [10]. Accordingly, a growing number of human studies have demonstrated an association between exposure to certain non-persistent pesticides and changes in circulating levels of reproductive hormones, particularly among occupationally exposed males [11], [12], [13], [14], [15], [16]. Despite this, epidemiological evidence on the effects of pesticides in current use on male reproductive system remains inconclusive.

Male anogenital distance (AGD), which is the distance from anus to scrotum, has been used as a measure of androgen status in experimental animals [10]. In human males, testicular volume (TV) and penile length have traditionally been used as indicators of androgenicity [17], and use of AGD has been rare [18]. However, recent epidemiological studies suggest that in utero exposure to anti-androgenic compounds may be associated with shortened AGD [18], [19], whilst shorter AGD may predict poorer testicular function in adult men [20], [21].

The effects of environmental and occupational exposure to pesticides on male reproductive system are of continuing concern. Developing countries account for one third of global pesticide consumption. In 2008, Brazil became the world’s largest consumer [22], with continued use of active ingredients already banned in other countries. Serra Gaúcha is a mountainous region in the South of Brazil settled by German and Italian immigrants characterized by family farms producing fruit, mostly grapes for wine production. The present study aimed to: 1) investigate the association of occupational exposure to modern pesticides with reproductive hormone levels, sperm quality, and TV among rural and urban young men residents from this region, and 2) examine reproductive hormone levels, sperm quality, and AGD and TV measurements in relation to potential gestational exposures, including maternal farming and smoking during pregnancy.

Section snippets

Study design and population

A cross-sectional study was conducted between 2012 and 2013 with a random sample of men aged 18–23 years from the agricultural population of the municipality of Farroupilha, in Rio Grande do Sul, the southernmost state of Brazil. A control group of the same age was selected from the urban area of the town. Considering a population of about 800 men in the age group of 18–23 years residing in the rural area of Farroupilha, a prevalence of acute pesticide exposure in the rural population of 7%, a

Results

Rural men were younger than urban men (64% of rural men were 18–20 years old versus 39% of urban men), while urban ones were more likely to have a higher education (Table 1). Most rural men were farmers at the time of the interview and had been employed the last three months. Very few participants reported current smoking, all from the rural area. About 25% of subjects reported feeling stressed, mostly those from the urban area, and one third of both rural and urban males were overweight or

Discussion

The present study investigated reproductive hormone levels, sperm quality, and genital measures in rural compared to urban young men in the South of Brazil, examining their association with occupational exposure to agricultural pesticides. The main findings were 1) the linear dose-response relationship poorer sperm morphology and lifetime use of all pesticides, fungicides, insecticides, herbicides, OP insecticides, dithiocarbamates and other chemical classes, mancozeb, glyphosate, and paraquat;

Conclusion

The present data suggest that chronic occupational exposure to modern pesticides, particularly herbicides and fungicides, may adversely affect semen quality in young male farmers in the South of Brazil, potentially leading to poorer morphology. Data also suggest that exposure to agricultural pesticides may acutely increase prolactin and chronically alter sex hormone levels acting at the pituitary level through prolactin and LH suppression, hampering compensatory responses to testicular

Conflict of interest

None.

Acknowledgements

This work was partially supported by the Ministry of Health, the Brazilian National Research Council (CNPq) and the CAPES (“Coordenação de Aperfeiçoamento de Pessoal de Nível Superior”). Cleber Cremonese had a CAPES predoctoral grant and Camila Picolli had a CAPES master’s degree grant. Rosalina Jorge Koifman and Fabio Pasqualotto are supported by the CNPq (“Bolsa de Produtividade em Pesquisa”). Carmen Freire had a “Jovens Talentos” grant from the CAPES/CNPq (Science Without Borders Program,

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    1

    Deceased 21 May 2014.

    2

    Cleber Cremonese and Carmen Freire contributed equally to this paper.

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