Urinary concentrations of parabens and reproductive parameters in young men

Highlights

• Urinary paraben concentrations were quantified to estimate environmental exposure

• Semen quality and serum reproductive hormone levels were evaluated

• No associations between parabens and any of the reproductive parameters were observed

• Urinary paraben concentrations may not adversely impact male reproductive function

Abstract

Parabens are a group of alkyl esters of p-hydroxybenzoic acid that are commonly added to personal care products, cosmetics, pharmaceuticals and beverage and food processing as antimicrobial preservatives. Parabens have been reported to show estrogenic effects and affect male reproduction function in animal models, but human epidemiologic studies are still scarce. The objective of this study was to examine associations between urinary concentrations of parabens and semen quality and reproductive hormone levels. This was a cross-sectional study with 215 young university students (18–23 years old) recruited between 2010 and 2011 in Southern Spain (Murcia Region). All men provided a urine, blood and semen sample on a single day. Urinary paraben concentrations (methylparaben, ethylparaben, propylparaben and butylparaben) were measured by dispersive liquid–liquid microextraction and ultra-high performance liquid chromatography with tandem mass spectrometry detection. Semen quality was evaluated by measuring volume, sperm concentration, total sperm count (TSC), motility and morphology following WHO guidelines. Serum samples were analyzed for reproductive hormones, including follicle-stimulating hormone, luteinizing hormone, testosterone, inhibin B and estradiol using immunoassays. Associations between urinary concentrations of parabens and semen quality parameters and reproductive hormone levels were examined using linear regression, adjusting for potential covariates. Ninety-four percent of the men had detectable urinary concentrations of parabens. After taking into account important covariates, urinary concentrations of parabens or their molar sum were not significantly associated with any semen parameters or any of the reproductive hormone levels. Relative to men in the lowest quartile of sum of urinary paraben concentrations, the adjusted difference (95% CI) of TSC (millions) for men in the 2nd, 3rd, and 4th quartiles were 4.1% (− 37.1;45.3), − 1.6% (− 41.9;38.8), and − 9.8% (− 52.5;32.8), respectively (P-trend = 0.55). Our results suggest that, in young men, urinary parabens may not adversely impact reproductive function, but further research is warranted to confirm these findings in other male populations.

Introduction

Parabens are a group of alkyl esters of p-hydroxybenzoic acid that are commonly added to personal care products, cosmetics, pharmaceuticals and beverage and food processing as antimicrobial preservatives (Andersen, 2008). Widespread human exposure to parabens is through dermal contact, inhalation or ingestion and are excreted via urine (Calafat et al., 2010, Frederiksen et al., 2011, Janjua et al., 2008). International biomonitoring studies have shown that parabens exposure is common among different populations, with detectable concentrations in the urine of most of the people tested (Calafat et al., 2010, CDC (Centers for Disease Control and Prevention), 2015, Moos et al., 2015).

Parabens are thought to have relatively low toxicity (Golden et al., 2005, Soni et al., 2005), and have been reported to show weak estrogenic and anti-androgenic effects in in vitro and animal studies (Chen et al., 2007, Darbre and Harvey, 2008, Gomez et al., 2005, Prusakiewicz et al., 2007, Satoh et al., 2005, Sun et al., 2016, Taxvig et al., 2008). A number of experimental studies have investigated the actions of parabens on male reproductive outcomes, showing that exposure to parabens negatively affects male reproductive system and spermatogenesis in mice or rats (Kang et al., 2002, Oishi, 2002a, Oishi, 2002b). Conversely, Hoberman et al. (2008) or Oishi (2004) found lack of effect of parabens on reproductive parameters in rodents. Only a very few studies have explored the associations between urinary concentrations of parabens and male reproductive function among humans, thus available information is still scarce. Three cross-sectional studies of male partners of subfertile couples attending infertility clinics examined this question. Meeker et al. (2011) and Nishihama et al. (2017) found no associations between urinary concentrations of parabens and semen parameters or reproductive hormone levels; but recently Jurewicz et al. (2017) reported significant inverse associations between urinary parabens concentrations and sperm morphology and motility and serum testosterone levels. Recently, urinary paraben concentrations were not associated with serum testosterone levels in male adolescents (12–19 years) participating in the National Health and Nutrition Examination Survey (NHANES) 2011–2012 (Scinicariello and Buser, 2016).

However, to the best of our knowledge, there are no studies exploring associations between parabens exposure and reproductive function in men non-selected for testis function or unaware of their fecundity. Therefore, the aim of this study was to assess the associations between urinary concentrations of parabens and semen quality and serum reproductive hormone levels in young men.