1. Introduction
The prevalence of obesity has almost tripled globally since 1975 and is continuing to rise [
1]. Obesity across the lifespan has been linked to many chronic health conditions, including diabetes, osteoarthritis, dyslipidemia, cardiovascular disease, and certain cancers [
2]. Although obesity is commonly attributed to high caloric intake, genetic predisposition, and sedentary lifestyles, mounting evidence suggests that environmental exposures to synthetic chemicals in consumer products may also contribute to obesity trends [
3,
4]. Specifically, increased exposure to certain endocrine-disrupting compounds, which have been termed “obesogens”, may promote or cause obesity by disrupting lipid metabolism or altering hormone levels [
3,
4,
5].
One such chemical that has received a notable amount of attention as a potential obesogen is bisphenol-A (BPA) [
6]. BPA is a synthetic monomer used in epoxy resins and polycarbonate plastics as a protective coating to prevent contamination or extend product shelf life and is found in a variety of consumer products including plastic food packaging, reusable food containers, canned goods, bottle tops, baby bottles, dinnerware plastics, and water supply pipes [
6,
7]. Exposure to BPA is widespread, with detectable levels of BPA in 89.7% of urine samples collected in the United States (U.S.) between 2011 and 2012 [
8]. The chemical structure of BPA is remarkably similar to synthetic estrogen and BPA can activate estrogen receptors and interfere with endocrine signaling even at low doses [
9]. This estrogen-like activity interferes with the production, release, transport, and metabolism of natural hormones, alters energy balance and fat gain, and is associated with reproductive and developmental toxicity [
3,
7,
10]. Despite this evidence, BPA has not been widely replaced in many food packaging sources and other consumer products, and worldwide production and consumption of BPA have increased over the past decade [
11].
The nation of Samoa has among the highest prevalence of obesity in the world with about 65% of the population having the condition [
12,
13]. Obesity trends have been largely attributed to changing dietary patterns, less active jobs, increasing costs of local staple food production, and more prevalent consumption of inexpensive, imported, micronutrient-poor, and energy-dense convenience foods [
12,
14]. Notably, these food products include a variety of processed canned foods, canned beverages, and foods wrapped in plastic packaging, many of which are low in nutritional content and are more likely to contain BPA [
15,
16].
Investigating the role of dietary BPA exposure may be important in identifying modifiable targets for intervention to reduce the burden of obesity and associated long-term health outcomes in Samoa and other vulnerable, low- and middle-income countries and communities. However, BPA exposure assessment for the study of chronic diseases is challenging. Specifically, biological monitoring, typically assessed with quantitative measurements of BPA concentrations in urine, reflects only recent exposure because BPA is rapidly metabolized and excreted with a half-life <7 h [
17]. Consequently, urinary BPA measurements collected from the same individual exhibit poor repeatability (among both adults and children), and therefore many samples collected over time are needed to accurately quantify usual exposure [
17,
18,
19]. Furthermore, BPA concentrations in blood samples, which reflect a longer window of exposure, are often low and difficult to detect [
20]. Since diet is the dominant source of BPA exposure [
21], a survey-based, self-report measure discriminating between high and low dietary exposure could be very useful, particularly for middle- and low-income countries and communities, because of issues related to affordability and access to laboratory testing. Therefore, the purpose of this study was to use a semi-quantitative, survey-based tool, designed for use in Samoa, to identify participant characteristics that are linked to higher estimated dietary BPA exposure and examine the relationship between BPA exposure and measures of adiposity in Samoan mothers and their children.
4. Discussion
This study was the first to characterize dietary BPA exposure scores and examine associations with measures of adiposity in Samoan mothers and children. This is an important area of investigation because, traditionally, low-income and underserved communities have been disproportionally exposed to environmental toxins [
31]. Diet in the Western Pacific, including Samoa, is marked by decreasing food self-sufficiency and increasing dependence on imported, packaged, and processed foods, which have been associated with increased BPA exposure [
7,
15]. There have been some efforts to phase out BPA in the U.S. [
32] as well as in New Zealand [
33] and the Philippines [
34], which are responsible for a large proportion of imported food in Samoa. However, BPA replacements in consumer products (e.g., bisphenol S and bisphenol F) share structural similarities and endocrine disrupting properties with BPA, and labeling of products as “BPA-free” may be misleading to consumers [
32]. Moreover, although BPA has been banned from use in baby bottles and formula containers in several countries [
34,
35], BPA is still used in many consumer goods, and the increased cost of BPA substitutes have largely isolated the focus of BPA phase-out to organic or more expensive food lines, leaving low-income communities disproportionately vulnerable to related adverse health effects [
36].
We identified both participant- and household-level characteristics associated with daily BPA indices. In both mothers and children, we observed lower daily BPA indices in the highest income homes. BPA levels have also been found to be inversely associated with family income in the U.S. [
37] and social class in Europe [
38]. However, in direct contrast to observations in these higher income countries [
39], increased income is associated with greater burden of obesity in Samoa [
39]. Historically, during economic progression in low- and middle-income countries, obesity has shifted from being more prevalent in high socioeconomic status groups to low socioeconomic status groups [
40]. Despite significant economic growth in Samoa over the last two decades, this shift has not been observed [
26]. In other settings, higher income is associated with a greater ability to purchase fresh foods but because there is a high reliance on farming across all income groups in Samoa, the relationships between socioeconomic status, dietary patterns, and health outcomes is more complicated [
23,
26,
41]. It is possible that socioeconomic status impacts adiposity via other pathways in this lower income setting and may be masking any impact of BPA or other environmental chemicals.
Next, in both mothers and children, we observed significant differences in BPA indices based on the level of physical activity, but in opposite directions. Specifically, we observed higher daily BPA indices in more active mothers but less active children. We initially suspected this association might be confounded by income in mothers but observed no difference in physical activity between the low income (<5000 talā) and the high income (≥10,000 talā) groups with 0 MVPA minutes reported in 76.1% and 78.3% of women, respectively. Nevertheless, the association with physical activity and daily BPA index was observed even when controlling for income in our regressions. In children, although the directionality of the association between higher BPA indices and lower physical activity was consistent with our hypothesis, this may be due to a small sample size of participants who were reported by their mothers to be “less active than their peers” (n = 33, 8.3%). There is a dearth of research related to BPA exposure and physical activity levels and additional work is needed to better understand this relationship in Samoa.
In children, we observed lower daily BPA indices in those categorized in the “less modern” dietary pattern group, compared to “more modern”. Children following a modern dietary pattern consume higher amounts of “westernized” foods including French fries, condiments, and snacks (i.e., processed, individually packaged items) compared with local foods such as vegetables, fish, and coconut [
23]. We did not have dietary pattern data in mothers to compare this finding. However, we observed a moderate to strong correlation between maternal and child BPA indices which is consistent with observations in a biomarker-based study of U.S. mothers and their children [
38] suggesting there may be a shared environmental or dietary factor that should be considered. These observations not only offer some corroboration to the BPA index applied here, but also represent a potential opportunity for intervention to reduce BPA exposure in the future (e.g., promoting more local, traditional diets in Samoa).
Despite identifying characteristics associated with dietary BPA exposure, we did not observe associations between dietary BPA indices and adiposity in this sample. In the U.S. and Canada, urinary BPA has been associated with increased odds of BMI-defined obesity in both children and adults even while controlling for covariates such as age, sex, and physical activity [
42,
43]. However, these observations were in higher income countries and, as noted above, there may be factors that are stronger drivers of adiposity in lower income settings such as Samoa. An additional factor that limits the comparability of this study to existing literature is the extreme adiposity observed in our sample. In mothers specifically, the mean BMI was 34.9 kg/m
2 with only 19.9% of the sample having a BMI <30 kg/m
2. This is quite different from comparable studies in higher income countries in which upwards of 75% of the sample had BMI in this range [
43]. Despite this, we did identify factors associated with adiposity in mothers and children. Age and socioeconomic status stand out in our results, though annual household income appears to be more important in mothers compared with total number of household assets in children.
While it is possible that dietary BPA exposure may not be as important a driver of adiposity in this sample as other factors, some limitations of this study should be considered in the interpretation of the results. First, detailed health histories of participants were not considered in our analyses. Because this was a community-based sample of mothers and children, participants were included despite a small proportion of mothers reporting diagnoses of hypertension or diabetes; potential associations between BPA exposure and adiposity comorbidities, particularly endocrine disorders, should be explored in the future. Next, the daily BPA index was computed using survey data from a dietary questionnaire and is therefore susceptible to recall bias and subsequent BPA index measurement error. Similarly, our questionnaire only covered the consumption patterns of the prior month; if this duration was not representative of typical dietary patterns, that could also contribute to exposure misclassification. However, the BPA-relevant questions were added to a food frequency questionnaire that was previously developed and validated to estimate long-term intake specifically for the Samoan population [
44]. Nevertheless, questionnaires covering a longer duration, or repeated administration of questionnaires over time, may provide more relevant information for obesity-related health outcomes [
24].
We relied on published measurements of BPA concentrations and expert raters to assign relative exposure scores, without any measurements of BPA in food or drinks directly consumed by participants. None of the quantitative studies that analyzed foods for BPA concentration and used to develop the exposure scores were conducted in Samoa, though a limited number were performed in New Zealand and China, countries with high imports to Samoa [
24]. BPA concentrations can vary across and within food/beverage items and BPA migration can be influenced by many factors [
24], [
45]. Nonetheless, the index was able to identify contrast in estimated dietary BPA exposure with variability across more than an order of magnitude. Finally, although the primary source of BPA exposure is diet [
21], unmeasured sources of BPA exposure not captured by a dietary questionnaire may be important in adverse health outcomes. Future work could include additional exploration and validation of the BPA exposure scores using human biospecimens from the Samoan population to identify potential non-dietary sources of BPA exposure and refine this survey-based tool for future use.