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Inverse associations between long-term weight change and serum concentrations of persistent organic pollutants

Abstract

There is emerging evidence that persistent organic pollutants (POPs) can increase the risk of various chronic diseases. As POPs mainly bioaccumulate in adipose tissue, weight change can affect serum concentrations of POPs. However, there are few population-based studies on effects of long-term weight change on serum concentrations of POPs. We examined associations between self-reported weight change over 1 year and 10 years and serum concentrations of seven POPs in 1099 adults aged 40. Serum concentrations of most POPs were higher in those with long-term weight loss, whereas they were lower in those with long-term weight gain. Adjusted correlation coefficients of each POP with weight change for 10 years were −0.23 (P<0.01) for trans-nonachlor, −0.16 (P<0.01) for p,p′-dichlorodiphenyldichloroethylene, and −0.21 (P<0.01) for β-hexachlorocyclohexane, −0.16 (P<0.01) for PCB169, −0.20 (P<0.01) for PCB180 and −0.17 (P<0.01) for 1,2,3,4,6,7,8-heptachlorodibenzo-p-dioxin. Weight change for 1 year showed similar but weaker associations, compared with those of long-term weight changes. Although both beneficial health effects after weight loss and harmful health effects after weight gain are generally expected, changes in serum concentrations of POPs in relation to weight change may act on health in directions opposite to what we expect with weight change.

Introduction

Persistent organic pollutants (POPs) are xenobiotics that mainly bioaccumulate in adipose tissue. Recent observational studies have found that environmental exposure to POPs is associated with various diseases including type 2 diabetes and cardiovascular diseases.1, 2 Importantly, it suggests that the effect of weight change on these diseases should be considered from two different viewpoints: effects of adipose tissue mass itself and effects of xenobiotics in adipose tissue. In particular, weight change can differently affect these two related factors. For example, weight loss reduces adipose tissue mass and improves related clinical variables. However, weight loss could be harmful if it leads to the release of xenobiotics from adipose tissue and increases serum POPs concentrations, because the released xenobiotics can reach critical organs through the circulation. Weight gain can act oppositely to weight loss.

Several small scale studies have reported that serum concentrations of some POPs increased after weight loss.3, 4, 5 However, most of these studies evaluated short-term changes in serum POPs concentrations after weight reduction programs that last several weeks or after surgery. Increase in serum POPs concentrations after weight loss may be transient, and could in the long run shorten half lives of POPs and eventually lower body burden of POPs. Furthermore, there are no studies about whether weight gain can lead to decreased serum concentrations of POPs.

Therefore, it is important to evaluate associations of serum concentrations of POPs in the general population over the full, long-term spectrum of weight change, ranging from weight loss to weight gain. In this study, we evaluated the associations between self-reported weight change during 1 year and 10 years before examination and serum concentrations of POPs concentrations at examination, using the US National Health and Nutrition Examination Survey.

Materials and methods

The 1999–2002 National Health and Nutrition Examination Survey conducted by the Centers for Disease Control and Prevention was designed to be nationally representative of the non-institutionalized, US civilian population. Serum concentrations of various biologically important POPs were measured in subsamples of the National Health and Nutrition Examination Survey 1999–2002 surveys. Information on self-reported weight 1 year and 10 years ago was obtained through interview. POPs were measured by high-resolution gas chromatography/isotope dilution high-resolution mass spectrometry at the Centers for Disease Control and Prevention. The POPs were reported on a lipid-adjusted basis using concentrations of serum total cholesterol and triglycerides. Although 49 POPs were measured in both National Health and Nutrition Examination Survey 1999–2000 and 2001–2002, many concentrations were below the level of detectability. Thus, we selected the seven POPs with the highest detection rate (trans-nonachlor, p,p′-dichlorodiphenyldichloroethylene, β-hexachlorocyclohexane, PCB169, PCB180, 1,2,3,4,6,7,8-heptachlorodibenzo-p-dioxin, 1,2,3,4,6,7,8-heptachlorodibenzofuran). There were 1099 study participants aged 40 years with information on serum concentrations of the seven selected POPs and weight change.

Because distribution of serum POPs concentrations was right skewed, log-transformed serum concentrations of POPs were used to examine associations with weight change in correlation analysis with adjustment for age, gender, race/ethnicity, poverty income ratio, cigarette smoking, alcohol consumption, exercise and current body mass index. We also examined adjusted geometric means of each POP by five categories of weight change to evaluate the trend in more detail. The categories of weight changes were <−5 kg (n=188), −5 kg to <−1 kg (n=258), −1 kg to <+1 kg (n=201), +1 kg to <+5 kg (n=260), and +5 kg (n=192) for weight change for 1year and <−10 kg (n=89), −10 kg to <−2 kg (n=184), −2 kg to <+2 kg (n=176), +2 kg to <+10 kg (n=356) and +10 kg (n=294) for weight change for 10 years. All statistical analyses were performed with SAS 9.1 and SUDAAN 9.0. Estimates of the main results were calculated accounting for stratification and clustering,6 adjusting for age, race–ethnicity instead of using sample weights; this adjustment has been regarded as a good compromise between efficiency and bias.6, 7 As results were very similar with SAS 9.1 and SUDAAN 9.0, we present the results based on SAS 9.1.

Results

Participants included 49.0% men and 55.1% white. Mean±s.d. for age was 60.2±13.0 (range 40–85). In general, serum concentrations of most POPs were higher in those with long-term weight loss, whereas they were lower in those with long-term weight gain. Adjusted correlations of 10-year weight change with POPs were on the order of −0.2 (Figure 1). Correlations with weight change for 1 year were also significant with most POPs, however strengths of associations were about half of those with weight change for 10 years. Figure 1 also shows adjusted means of serum concentrations of five POPs according to five categories of weight changes. When we did stratified analyses by gender, body mass index or cigarette smoking, the results were similar (data not shown).

Figure 1
figure1

Correlation coefficients (r) for 10 year weight change and geometric mean serum concentrations of POPs across categories of self-reported weight change over 1 year and 10 years before examination: Adjusted for age, gender, race/ethnicity, poverty income ratio, cigarette smoking, alcohol consumption, exercise and current body mass index. Abbreviations: HpCDD, 1,2,3,4,6,7,8-heptachlorodibenzo-p-dioxin; HpCDF, 1,2,3,4,6,7,8-heptachlorodibenzofuran; p,p′-DDE, p,p′-dichlorodiphenyldichloroethylene; wt, weight

Discussion

This study clearly showed that serum concentrations of POPs at examination were associated with previous weight change in the US general population. We interpret that weight loss can lead to increased serum concentrations of POPs, whereas weight gain can decrease them. These patterns were more strongly observed with weight change for 10 years than weight change for 1 year.

As the information on previous body weight used in this study was self-reported, inaccurate recall of previous body weight may distort true associations between weight change and serum concentrations of POPs. However, recalled weight strongly correlated with measured weight even though accuracy of recall could be influenced by various factors.8 Also, this type of error in this study is most likely random, not systemic, because participants did not know their serum concentrations of POPs when they reported their previous body weight. This type of error would tend to attenuate true associations. Also, possible associations between weight change and POPs were largely unknown to the participants as well as researchers. Therefore, at most, a small part of our observation on weight change and POPs may be explained by bias. In fact, the release of POPs from adipose tissue after short-term weight loss after weight reduction programs or surgery has already been observed in several small scale longitudinal studies.3, 4 Also, one study directly observed that increase in plasma pollutant levels in response to weight loss in humans was related to in vitro subcutaneous adipocyte basal lipolysis.5

In fact, many observational studies have reported that weight loss was associated with increased risk of cardiovascular disease, dementia or total mortality.9, 10, 11, 12, 13, 14 This finding has typically been interpreted as reflecting reverse causality due to unintentional weight loss from pre-existing illness or cigarette smoking, or loss of lean mass rather than fat mass. However, there have been some studies in which the excess risk in the weight loss group was observed even after excluding or adjusting for smoking and pre-existing conditions.12, 13 Furthermore, mild to moderate weight gain did not increase or even decreased coronary events in several epidemiological studies.11, 14 However, these puzzling findings on weight change from observational studies have been dismissed simply as bias because of no biological plausibility.15, 16

Our findings on the dynamics of POPs may be helpful in explaining these puzzling findings. In relation to weight changes, changes in adipose tissue mass itself and dynamics of POPs may act as countervailing forces. Epidemiologic observations of the net health effects of weight change may reflect a mixture of these two opposite effects. Also, the net effects may differ depending on health outcome. Pathogenesis of some health outcomes may be more affected by the change of adipose tissue mass, whereas pathogenesis of other health outcomes may be more affected by the change of serum concentrations of POPs. However, this study could not provide direct evidence on these speculations and future studies focusing on this issue are required.

Importantly, recent epidemiological studies have suggested that the background exposure to POPs might not be safe. Although the specific kinds of POPs differed depending on disease outcome, the exposure to POPs at low dose (at levels similar to the dose caused by current environmental exposure) were associated with increased risk of various common diseases such as type 2 diabetes, cardiovascular diseases, or cancer.1, 2 Therefore, researchers and clinicians need to consider lipophilic xenobiotics, such as POPs, that bioaccumulate in adipose tissue as well as obesity itself when they study or manage obesity issue because such xenobiotics may work against what we generally expect from weight loss or gain.

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Correspondence to D-H Lee.

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Lim, J., Son, HK., Park, SK. et al. Inverse associations between long-term weight change and serum concentrations of persistent organic pollutants. Int J Obes 35, 744–747 (2011). https://doi.org/10.1038/ijo.2010.188

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Keywords

  • adipose tissue
  • persistent organic pollutants (POPs)
  • weight gain
  • weight loss

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