Does heavy metals pollution affects semen quality in men? A case of study in the metropolitan area of Naples (Italy)

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Abstract

In recent years, a significant increase in the incidence of male infertility has been observed and described in the international literature, raising questions about its causes. Several authors have suggested that exposure to environmental pollution may contribute to a perceived decline in semen quality worldwide. Although several studies have been conducted about the effects on male fertility caused by exposure to heavy metals in the workplace, research on the effects caused by continued exposure to low doses of heavy metals pollution in urban areas is still scarce.

The aim of this study is to identify the relationships between high concentrations of heavy metals and male semen quality in the metropolitan area of Naples. We considered only those elements (Al, As, Cd, Cr, Cu, Hg, Mn, Mo, Pb, Sb, Tl, Zn) that previous studies have indicated as possible candidates to have some influence on human semen quality.

We measured semen quality among 600 subjects selected from a sample of 1237 men regularly examined at the Andrology Laboratory of the University of Naples “Federico II” for problems related to male fertility. Using statistical methods the semen data (semen volume, sperm concentration, sperm total count, sperm motility, pH) were compared with the geochemical distribution of heavy metals in soils of the Napoli metropolitan area.

Results show a strong correlation between anomalous Pb and Sb concentrations and men with poor semen quality. A weaker correlation was also observed with Hg and Zn while the anomalous concentration values of the other elements (Al, As, Cd, Cr, Cu, Mn, Mo and Tl) appear to have no correlation with poor quality of the human semen.

Highlights

► We studied the relationships between high concentrations of heavy metals and male semen quality. ► We measured semen quality among 600 subjects selected from a sample of 1237 men. ► The semen data were compared with the geochemical distribution of heavy metals in soils. ► We found a positive correlation between Pb and Sb concentrations in soils and reduced human semen quality. ► Anomalous concentrations of other elements in soils appear to have no correlation with semen quality.

Introduction

The international growth of industrial and agricultural production and the consequent increase in consumption of goods, caused an increase in exposure to various substances that are potentially harmful to humans. In recent years, many scientists focused their interest on heavy metals in the soils of urban areas where pollution might have a direct influence on public health. The exposure to some heavy metals has been associated to a huge variety of adverse health effects, including infertility (Akinloye et al., 2006, Benoff et al., 2000, De Rosa et al., 2003).

While some of these elements are essential for humans, relatively high levels of exposure can be harmful. Arsenic (As), cadmium (Cd), chromium (Cr), mercury (Hg) and lead (Pb) must be especially taken into account due to their potential toxic effects. Other elements such as aluminum (Al), antimony (Sb), copper (Cu), molybdenum (Mo), manganese (Mn), thallium (Tl) and zinc (Zn) must be also carefully considered if high concentrations are detected in a specific area.

A population is exposed to metals at low concentrations either voluntarily through supplementation or involuntarily through intake of contaminated food and water or contact with contaminated soil, dust, or air. Evidences gathered on humans and animals suggest that these metals may have adverse impacts on male reproductive health at relatively low levels.

Cadmium, for instance, has been linked to reduced human semen quality and DNA damage (Telisman et al., 2000, Xu et al., 2003), while it has been shown that Pb may adversely affect sperm shape, motility, and DNA integrity (Eibensteiner et al., 2005, Hernandez-Ochoa et al., 2005, Jurasovic et al., 2004, Telisman et al., 2007).

Lead exposure is one of the most prevalent occupational and environmental health problems. Lead effect on human male fertility has been postulated by observations published by Lancranjan et al. (1975). Many studies have also reported that decrease in semen quality may be present in groups of men with Pb exposure on the workplace (Alexander et al., 1996, Assennato et al., 1986, Kuo et al., 1997, Lerda, 1992, Wildt et al., 1983). Human data on non-occupational exposure to this metal is limited and epidemiological studies provided equivocal results concerning its effects on hormone concentration, male infertility and sperm parameters (Benoff et al., 2000).

Despite the fact that the actual causes of increased infertility remain controversial (Hovatta et al., 1998, Pant et al., 2003, Swan et al., 1997), several studies confirm that male sperm counts are declining and that environmental factors such as pesticides, heavy metals, estrogen-like substances and chlorinated compounds negatively impact spermatogenesis (Benoff et al., 2000, Cooper and Kavlock, 1997, De Rosa et al., 2003, Fredricsson et al., 1993, Watanabe and Oonuki, 1999). Carlsen et al. (1992) demonstrated a 45% drop in human sperm count, from an average of 113 million/mL of semen in 1940 to 66 million in 1990.

An estimated 6% of men in reproductive age show symptoms of infertility. The most frequent causes, accounting for 90% of the total, are associated with spermatogenesis. The other causes are related to alterations in sperm transport and accessory glands in the male genital tract (6%), erectile disorders (2%), ejaculatory disorders (1%), and functional alterations in the sperm and coitus (1%) (Jequier, 2002). There may be absence of sperm (azoospermia), a decrease in the number (oligozoospermia), alteration in form (teratozoospermia), in the motile capacity (astenozoospermia), or in the vitality (necrospermia) (Bigazzi, 1987).

The aim of the present study is to identify possible relationships between high concentrations of some heavy metals and male infertility in the metropolitan area of Naples. This study focuses only on those elements (Al, As, Cd, Cr, Cu, Hg, Mn, Mo, Pb, Sb, Tl, Zn) that previous researches have indicated to have some influence on the quality of human semen (Benoff et al., 2000, De Rosa et al., 2003, Meeker et al., 2008, Telisman et al., 2000, Telisman et al., 2007).

Section snippets

Study area

The metropolitan area of Napoli is a typical example of how intense human activities can be affected by various environmental hazards, such as hydrogeological degradation, soil and water pollution, as well as volcanic, seismic and bradyseismic activities. The Naples area is located in the Campania Region along the Tyrrhenian coastline, in one of the most densely populated (more than 3 million inhabitants) active volcanic areas on Earth. The transportations network expanded considerably in the

Semen analysis

We enrolled in the study 1237 subjects living in the metropolitan area of Naples, who were treated for problems related to male fertility at the Andrology Laboratory of the Department of Molecular and Clinical Endocrinology and Oncology, University of Naples “Federico II”. A detailed questionnaire was completed by a specialist in andrology for each of the 1237 subjects. The information collected during the interview is related to age, smoking habits, alcohol consumption, and professional and

Semen quality

Seventy percent of the subjects do not smoke and have a median age of 30 years. The mean semen volume for the entire group was 2.8 mL with a minimum value of 0.1 mL up to a maximum value of 7.8 mL and a standard deviation 1.1 mL (Table 2); 28% of subjects had a semen volume lower than or equal to 2 mL (WHO reference value) and the remaining 72% a volume above this value (Fig. 5A).

In all samples the average (mean) percentage of motile sperm was 25.7%, significantly below the WHO reference value (≥ 50%)

Conclusion

Although it is well recognized that the evaluation of semen quality alone is not a good tool to study male fertility potential, the measure of sperm parameters is usually used as a good marker of male fertility. In fact male fertility should be related not only to endocrine and systemic diseases but also to parity and educational level, habits and lifestyles.

On the other hand, sperm parameters can be modified by many common variables, as age, time of abstinence, smoking habit, alcohol and drugs

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