Occupational exposure to pesticides and consequences on male semen and fertility: A review

Highlights

• Exposure to pesticides induces reproductive hormonal changes.

• Sperm's DNA damage may occur in exposure to pesticides.

• DDT and its metabolites have estrogenic effects on males.

• Well-designed long-term studies are needed to explore full effects.

Abstract

Exposure to pesticides affects many body organs including reproductive system. Disorder of the reproductive system leads to infertility and therefore has been in the center of attention within the recent decades.

Pesticides are one of the compounds that might reduce the semen quality in the exposed workers according to current knowledge. Although many underlying mechanisms have been proposed, the mechanisms of action are not clarified yet. The object of the present review was to criticize all the results of studies which evaluated the pesticide effects on male reproductive system. Results indicate that semen changes are multifactorial in the workers exposed to pesticides as there are numerous factors affecting sperm quality in occupational exposures. Majority of pesticides including organophosphoruses affect the male reproductive system by mechanisms such as reduction of sperm density and motility, inhibition of spermatogenesis, reduction of testis weights, reduction of sperm counts, motility, viability and density, and inducing sperm DNA damage, and increasing abnormal sperm morphology. Reduced weight of testes, epididymis, seminal vesicle, and ventral prostate, seminiferous tubule degeneration, change in plasma levels of testosterone, follicle-stimulating hormone (FSH), and luteinizing hormone (LH), decreased level and activity of the antioxidant enzymes in testes, and inhibited testicular steroidogenesis are other possible mechanisms. Moreover, DDT and its metabolites have estrogenic effects on males. Although effect of pesticides on sperm quality is undeniable, well-designed long-term studies are needed to elucidate all the possible affecting variables such as socioeconomic, cultural, nutritional, occupational, physical, and clinical characteristics alongside pesticides.

Introduction

Agriculture is a source of economic income especially in the developing countries. Farm workers may have contact with many substances with potential hazards, of the most common of which, are pesticides and particularly the organophosphorus (OP) compounds (Mostafalou and Abdollahi, 2013a, Mostafalou and Abdollahi, 2013b).

Of the known causes of infertility are occupational exposures to harmful environmental factors (Table 1). Since many of these potential hazards exist in the environment, occupational exposures are not easy to be proved. However, the decreased fertility rate in certain occupations is much more significant than what is expected among the general population (Ashiru and Odusanya, 2009). Unfortunately, chronic or low-level exposures are not defined and this makes it difficult to determine different classes of exposures in the studies (Peiris-John and Wickremasinghe, 2008). Peiris-John and Wickremasinghe (2008) tried to determine whether exposure to OPs, at levels lower than that result in clinical manifestations of acute OP poisoning, leads to any adverse impact on fertility, growth and development. They suggested that OP exposure has a greater impact on fetal and infant growth and development than on adults when exposed to the same concentrations of pesticides and meanwhile raised concerns regarding exposure levels currently considered as safe level for human reproductive function.

Occupational exposure occurs while mixing, loading, spraying, and assessment of the pesticides (Shadnia et al., 2005, Mekonnen and Ejigu, 2005). There are different types of occupational hazards affecting reproductive organs in both males and females (Table 1). But, male reproductive activity is highly sensitive to many man-made chemicals and physical agents produced by agricultural and industrial activities (Ashiru and Odusanya, 2009).

Female or male infertility is the reason for involuntary sterility in 39% and 20% of the cases, respectively; in 26% of the cases, the reason is found in both men and women. The clinicians cannot identify the cause of infertility in 15% of the cases (idiopathic sterility) (Winker and Rüdiger, 2006). Infertility is not limited to Western countries; it is a global phenomenon involving developing countries, as well (Clementi et al., 2008). Subfertility is another phenomenon regarded to be idiopathic in most men (Bretveld et al., 2007) and can be influenced by several factors such as lifestyle, occupational exposure, environmental exposure, and other conditions listed in Table 1. Regarding the possibility of occupational exposure to pesticides, some protection guidelines have been described in details but they are not always adhered (Table 2).

A pesticide is defined as “any substance or combination of substances used to prevent or eradicate unwanted insects including vectors of diseases in human-beings and animals, weeds, fungi, or animals in order to enhance food production and help production processing, storage, transport, or marketing of the food and agricultural commodities” (Abdollahi et al., 2004, Clementi et al., 2008, Shadnia et al., 2005, Sifakis et al., 2011). Pesticides act as endocrine disrupting chemicals (EDCs). The EDC is defined by US environmental protection agency (EPA) as “an exogenous agent that is potentially capable of synthesis, secretion, transport, binding, action, or elimination of the natural hormones responsible for the maintenance of homeostasis, reproduction, and developmental processes in the body” (Sifakis et al., 2011).

Many pesticides exist with hundreds of trade names. In 66% of the cases, they are used in agriculture (De Silva et al., 2006). It has been estimated that almost 1844 commercially used pesticide compounds are available in the US market and almost 750,000 people experience new exposure to them annually (Perry, 2008).

Inhalational, dermal, oral, and placental exposures can occur (Gilden et al., 2010). The results of an exposure may manifest immediately (Talaie et al., 2012), at a later stage, and sometimes descending to subsequent generations, although genetic polymorphism has an important role in this regard (Sifakis et al., 2011). Besides, the effects can be reversible, permanent, or even trans-generational and take place in the offspring as exposure can occur during pregnancy and intrauterine life, childhood, or later on (Sifakis et al., 2011). Pesticides contaminate the environment, soil, and agricultural products. As a result, human beings are exposed to the pesticides through food, water, air, tainted breast milk, playing in the fields, or skin contact. Pesticides may differ according to their chemical structure, mechanism of action, and the toxicity they exhibit; but, each pesticide typically consists of one (or more) active ingredient. Individuals are often exposed to a mixture of toxicants and not a single agent. Effects of the ingredients of this mixture may be synergistic or antagonistic (Sifakis et al., 2011). The study of adverse effects of pesticides on human reproduction system backs to more than 3 decades ago (Shojaei Saadi and Abdollahi, 2012a, Shojaei Saadi and Abdollahi, 2012b). Pesticide exposure has increased the concern about their potential hazards to the health including acute and chronic poisonings (Mostafalou and Abdollahi, 2013a, Mostafalou and Abdollahi, 2013b). It is generally a health problem especially in poor rural populations where people of all both sexes and all ages live and work near the fields on which chemicals are applied (10). Moreover, it has adverse effects on central nervous, immune, endocrine, and reproductive systems (Shojaei Saadi and Abdollahi, 2012a, Shojaei Saadi and Abdollahi, 2012b). In this regard, three major routes of exposure to pesticides have been identified: (Ashiru and Odusanya, 2009) occupational, ((Peiris-John and Wickremasinghe, 2008) environmental (Shadnia et al., 2005, Saeidnia and Abdollahi, 2013), and dietary exposures (Clementi et al., 2008). Occupational exposure to various risk factors is generally more common than the environmental exposure (Ashiru and Odusanya, 2009).