Adipose tissue concentrations of persistent organic pollutants and total cancer risk in an adult cohort from Southern Spain: Preliminary data from year 9 of the follow-up

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Abstract

There is an increasing trend in the incidence of cancer worldwide, and it has been accepted that environmental factors account for an important proportion of the global burden. The present paper reports preliminary findings on the influence of the historical exposure to a group of persistent organic pollutants on total cancer risk, at year 9 in the follow-up of a cohort from Southern Spain.

A cohort of 368 participants (median age 51 years) was recruited in 2003. Their historical exposure was estimated by analyzing residues of persistent organic pollutants in adipose tissue. Estimation of cancer incidence was based on data from a population-based cancer registry. Statistical analyses were performed using multivariable Cox-regression models.

In males, PCB 153 concentrations were positively associated with total cancer risk, with an adjusted hazard ratio (95% confidence interval) of 1.20 (1.01–1.41) for an increment of 100 ng/g lipid.

Our preliminary findings suggest a potential relationship between the historical exposure to persistent organic pollutants and the risk of cancer in men. However, these results should be interpreted with caution and require verification during the future follow-up of this cohort.

Introduction

There is an increasing trend worldwide in the incidence of cancer, and predictions for 2030 include annual rates of 27 million incident cases of cancer and 17 million cancer-related deaths annually (Ferlay et al., 2010, International Agency for Research on Cancer, 2008). This trend cannot be solely explained by the improvement in diagnostics or by the aging of populations. In addition, wide disparities in the incidence of the most frequent types of cancer have been reported across the five continents, possibly due to complex interactions between genetic susceptibility and modifiable risk factors (Kamangar et al., 2006).

It has traditionally been accepted that environmental factors account for a large proportion of cancers, reaching up to 80–90% of the global burden of the disease (International Agency for Research on Cancer, 2008). Specifically, an estimated 6% of total cancer deaths is attributable to occupational or environmental exposure to carcinogenic agents, which appears to be a small percentage in comparison to other known causes, such as tobacco consumption, but translates into a large number of individuals in the general population (American Cancer Society, 2014). Furthermore, little is known about the health outcomes derived from exposure to complex mixtures of environmental pollutants that can interact with each other and with internal elements of the organism (American Cancer Society, 2014, Kortenkamp, 2006). In this regard, the European Code against Cancer emphasized the need to apply strict regulations aimed at preventing any exposure to known cancer-causing substances in order to decrease the cancer risk (Boyle et al., 1995).

Organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) are persistent organic pollutants (POPs), i.e., highly lipophilic chemicals that are very resistant to degradation and tend to accumulate and biomagnify in food chains, resulting in the considerable exposure of living organisms (UNEP, 2003). OCPs have been used in many agricultural activities and as vector control (Porta et al., 2002), while PCBs have been employed as dielectric and heat exchange fluids, among other commercial applications (WHO, 2000). Although the use of most OCPs and PCBs has been banned or severely restricted in most countries, these chemicals are still detected in virtually all human populations and environmental matrices, and diet (especially fatty food) has been reported to be the main route for human exposure (Bräuner et al., 2012a).

There is increasing scientific evidence that exposure to low levels of POPs, such as those occurring in the general population, is related to an increased risk of several adverse health effects, including some of the most prevalent types of cancer, e.g. hepatocellular carcinoma (Zhao et al., 2011), breast cancer (Salehi et al., 2008), cancer of the head and neck (Govett et al., 2011), non-Hodgkin lymphoma (Engel et al., 2007), prostate cancer (Xu et al., 2010), testicular germ cell tumors (McGlynn et al., 2008), or pancreatic cancer (Hardell et al., 2007). Additionally, long-term occupational exposure to PCBs has been associated with elevated melanoma mortality (Ruder et al., 2014). However, there have been conflicting reports on the relationship between exposure to low levels of POPs, such as those occurring in the general population, and cancer risk, with some studies reporting positive associations but many others finding no evidence to support a causal association (Cassidy et al., 2005, Charlier et al., 2003, Cohn et al., 2010, Gatto et al., 2007, Govett et al., 2011, Hardell et al., 2006, Hoyer et al., 2001, Laden et al., 2001, Lopez-Carrillo et al., 2002, Lopez-Cervantes et al., 2004, Mozzachio et al., 2008, Pavuk et al., 2004, Recio-Vega et al., 2011, Snedeker, 2001, Soto and Sonnenschein, 2010, Svensson et al., 1995, Ward et al., 2000, Wolff et al., 2000, Xu et al., 2010).

The present paper reports preliminary results on the influence of the historical exposure to a group of organochlorine pesticides and polychlorinated biphenyls on total cancer risk, at year 9 during the follow-up of an adult cohort from Southern Spain.

Section snippets

Study cohort

The present research is part of a hospital-based study that aimed to characterize the exposure to POPs of an adult cohort from Southern Spain and assess potential health outcomes. The study design, recruitment, and methods have been extensively described elsewhere (Arrebola et al., 2009, Arrebola et al., 2010, Arrebola et al., 2013a). In brief, Granada province covers an area of 12,635 km2 in Southern Spain. Study subjects were recruited in two public hospitals, San Cecilio University Hospital

Results

Out of the 368 adults enrolled in this study, 22 were diagnosed with cancer (Table 2), i.e., a cumulative incidence of 6%. Median follow-up time, including censored and non-censored data, was 75.1 months both in men and women. Incidence density in our population was 83.93 × 10 5 person–years. Table 2 shows the classification of cancer incident cases according to tumor site. Females showed a cumulative incidence of 5%, an incidence density of 69.77 × 10 5 person–years, and the most common tumor

Discussion

In the present preliminary study, total cancer risk in men was associated with concentrations of PCB 138 (statistically significant) and PCB 153 (borderline significant) in an apparently monotonic manner. In men, we observed a rise in cancer risk of 20% (95% CI: 1–41%) for an increase of 100 ng/g lip in adipose tissue PCB 153 concentrations. The fact that these associations were not found in women might be due to the lower number of female cases or because of sex-related physiological

Conflict of interest

The authors declare no conflict of interest.

Acknowledgments

The authors gratefully acknowledge scientific and technical assistance provided by Richard Davies. Dr J.P. Arrebola is currently receiving a postdoctoral contract from the Consejería de Igualdad, Salud y Políticas Sociales, Junta de Andalucía (RH-0092-2013). The results would not have been achieved without the selfless collaboration of the staff from Santa Ana and San Cecilio Hospitals and the patients who took part in the study.

This study was supported in part by research grants from the

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