Decreased plasma levels of perfluoroalkylated substances one year after bariatric surgery

Highlights

• Plasma levels of 17 PFASs were analyzed before and one year after bariatric surgery.

• Levels of all analyzed PFASs and concentrations of serum proteins decreased significantly.

• Associations between levels of PFAS and proteins were not supported in regression analyses.

• Decreased PFAS levels may be influenced by a reduced food intake and changed absorption.

Abstract

Per- and polyfluoroalkylated substances (PFASs) are classified as persistent organic pollutants (POPs), and known to be protein bound. The aim of the present study was to determine the levels of 17 different PFASs before and one year after bariatric surgery, and to assess whether weight loss and changed serum protein concentrations could be influencing factors. Plasma samples from 63 patients were analyzed for nine perfluoroalkyl carboxylic acids (PFCAs), three perfluoroalkane sulfonic acids (PFSAs), and five perfluoroalkyl sulfonamide based substances (PASF) before and after surgery. Protein determination was performed in the corresponding serum samples. Mean weight loss one year after surgery was 32.1 kg. The plasma levels of all PFASs decreased with 4–34% compared to preoperative values, and included perfluorononanoic acid (PFNA), perfluorodecanoic acid (PFDA), perfluoroundecanoic acid (PFUnDA), and perfluorobutane sulfonate (PFBS), which have been identified with increasing levels in the general population during recent years. Serum protein concentrations also decreased with 7–8%. Although protein levels were positively correlated with PFOA, PFBS, PFHxS and PFOS, regression analysis revealed that neither weight loss nor reductions in concentrations of serum protein could explain the decreased PFAS levels. The type of surgical procedure did not influence the changes of PFAS levels between the two sample points. A reduced food intake and alterations in absorptions of nutrients after bariatric surgery may have influenced the observed decreasing plasma levels of PFASs.

Introduction

Globally, 39% of the adult population were overweight in 2016, and 13% were obese (WHO, 2016). Overweight and obesity are defined as abnormal or excessive fat accumulation that may impair health (WHO, 2017). Among comorbidities of overweight and obesity are type 2 diabetes (T2D), cardiovascular disease, asthma, arthritis, and certain forms of cancer (Mokdad et al., 2003; Sjostrom, 1992a, Sjostrom, 1992b). A growing number of bariatric surgeries are being performed as treatment for obesity (Angrisani et al., 2015), and long term improvements in cardiovascular risk factors and obesity related comorbidities are reported after surgery (Jakobsen et al., 2018; Sjostrom et al., 2004).

The different types of surgical procedures are either restrictive, malabsorptive, or a combination of both (Stein et al., 2014). Depending on the type of surgery, the anatomical and physiological changes introduced in the gastrointestinal tract affect absorption and bioavailability of nutrients, minerals, trace elements, vitamins, and drugs (Sawaya et al., 2012; Stein et al., 2014). Bariatric surgery can give rise to negative health effects, such as postoperative complications and misuse disorders (Arterburn and Courcoulas, 2014; Jakobsen et al., 2018; Peterhansel et al., 2013), as well as an increased risk of macro- and micronutrient deficiencies, including protein deficiency (Stein et al., 2014; Verger et al., 2016).

Per- and polyfluoroalkyl substances (PFASs) are anthropogenic substances, which have been manufactured since the 1950s (Lindstrom et al., 2011). PFASs are characterized by thermal and chemical stability, and surfactant properties, like water- and oil repellency. The substances are therefore used in products like food containers, textile coatings, leather, cement, cosmetics, polishes, waxes, insecticides and fire-fighting foams (Kissa, 2001). PFASs are also present in the environment, due to adsorption to soil and groundwater (Backe et al., 2013; Kucharzyk et al., 2017). They are resistant to degradation, and have long half-lives in humans (Eriksson et al., 2017; Lindstrom et al., 2011; Olsen et al., 2007; Zhang et al., 2013). Despite the wide range of PFASs used in different industrial products, only perfluorooctane sulfonate (PFOS) is listed in the Stockholm Convention. Perfluorooctanoic acid (PFOA) is recommended for listing, while perfluorohexane sulfonate (PFHxS) is under consideration by the Persistent organic pollutants (POPs) Review Committee (SC, 2016).

Human exposure to PFASs may occur via various sources, such as food, consumer products, drinking water, and inhalation of ambient air (D'Eon J and Mabury, 2011; Haug et al., 2011), and PFASs have been detected in human blood, breast milk, brain, liver and other organs (Haug et al., 2011; Perez et al., 2013; Stahl et al., 2011). The most studied PFASs, PFOA and PFOS, are poorly metabolized in mammals (Stahl et al., 2011). The elimination of PFASs from the body is assumed to follow a first-order kinetic process (Kissa, 2001). In humans, the renal clearance of PFASs is low compared to other species (Harada et al., 2005; Stahl et al., 2011). For women, menstruation, pregnancy, and breast feeding may also serve as excretory routes (Harada et al., 2005; Thomsen et al., 2010; Winkens et al., 2017; Yang et al., 2016).

The scientific literature suggests that exposure to PFASs is associated with disturbances of the immune system (Dalsager et al., 2016; Grandjean et al., 2012; Grandjean et al., 2017) and thyroid hormone system (Melzer et al., 2010; Shrestha et al., 2015), and also alterations in sexual maturation (Lopez-Espinosa et al., 2011). Further, associations with indicators of metabolic syndrome (Lin et al., 2009), and a higher risk of T2D (Sun et al., 2018), as well as development of childhood overweight and obesity (Braun et al., 2016; Lauritzen et al., 2018) have been reported. Recently, a diet-induced weight-loss trial showed that higher baseline levels of PFAS were associated with a greater weight regain in women (Liu et al., 2018) suggesting that PFASs may also interfere with weight regulation in humans.

In contrast to several other POPs, such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and dichlorodiphenyltrichloroethane (DDT), which are lipophilic and accumulate in fat tissues, most PFASs are weakly lipophilic and water soluble with binding affinity mainly to albumin, and to a lesser extent, other proteins (Bischel et al., 2011; Jones et al., 2003; Kucharzyk et al., 2017; Luebker et al., 2002). Increased circulating levels of lipophilic POPs after bariatric surgery have been reported from several studies (Dirinck et al., 2016; Dirtu et al., 2013; Jansen et al., 2018; Kim et al., 2011; Rantakokko et al., 2015). To our knowledge, only one research group has previously studied changes in the circulating levels of PFAS after bariatric surgery, showing minor changes (both increase and decreases) one year after surgery (Rantakokko et al., 2015).

Apparently, changes in plasma levels of PFAS after weight loss are still insufficiently investigated. The aim of the present study was to determine the levels of a broad spectrum of PFASs before and one year after bariatric surgery, and furthermore to study if changes in serum protein concentrations or body weights were important determinants for postoperative PFASs changes.