BackgroundAverage profiles of salivary progesterone in women vary significantly at the inter- and intrapopulation level as a function of age and acute energetic conditions related to energy intake, energy expenditure, or a combination of both. In addition to acute stressors, baseline progesterone levels differ among populations. The causes of such chronic differences are not well understood, but it has been hypothesised that they may result from varying tempos of growth and maturation and, by implication, from diverse environmental conditions encountered during childhood and adolescence.Methods and FindingsTo test this hypothesis, we conducted a migrant study among first- and second-generation Bangladeshi women aged 19–39 who migrated to London, UK at different points in the life-course, women still resident in Bangladesh, and women of European descent living in neighbourhoods similar to those of the migrants in London (total n = 227). Data collected included saliva samples for radioimmunoassay of progesterone, anthropometrics, and information from questionnaires on diet, lifestyle, and health. Results from multiple linear regression, controlled for anthropometric and reproductive variables, show that women who spend their childhood in conditions of low energy expenditure, stable energy intake, good sanitation, low immune challenges, and good health care in the UK have up to 103% higher levels of salivary progesterone and an earlier maturation than women who develop in less optimal conditions in Sylhet, Bangladesh (F 9,178 = 5.05, p < 0.001, standard error of the mean = 0.32; adjusted R 2 = 0.16). Our results point to the period prior to puberty as a sensitive phase when changes in environmental conditions positively impact developmental tempos such as menarcheal age (F 2,81 = 3.21, p = 0.03) and patterns of ovarian function as measured using salivary progesterone (F 2,81 = 3.14, p = 0.04).ConclusionsThis research demonstrates that human females use an extended period of the life cycle prior to reproductive maturation to monitor their environment and to modulate reproductive steroid levels in accordance with projected conditions they might encounter as adults. Given the prolonged investment of human pregnancy and lactation, such plasticity (extending beyond any intrauterine programming) enables a more flexible and finely tuned adjustment to the potential constraints or opportunities of the later adult environment. This research is the first, to our knowledge, to demonstrate a postuterine developmental component to variation in reproductive steroid levels in women.

Women living in energetically stressful conditions have significantly lower baseline salivary steroid levels compared to those in affluent environments. Developmental hypotheses suggest that interpopulation variation in ovarian function results from contrasting environments experienced during growth. We use a migrant study of Bangladeshi women to test this hypothesis. We compared middle-class women (19-39 years) who migrated to London, UK, at different life-stages (pre and postmenarche), with Bangladeshi sedentees, second-generation British-Bangladeshis, and white British women living in similar London neighborhoods (total n = 227). We analyzed levels of salivary estradiol for one menstrual cycle, together with data on anthropometry, diet, lifestyle, and migration and reproductive histories. Results from multiple linear regression models, controlling for anthropometric and reproductive variables, show no significant differences in baseline estradiol levels between groups whether all cycles or just ovulatory cycles are analyzed. We also found no correlation between age at migration or time since migration on estradiol levels, nor between adult estradiol levels and age at menarche. Our results differ from previous reports of significantly lower salivary estradiol levels in populations living in more extreme ecological settings. They also contrast with our previous findings of significant intergroup differences in baseline levels of salivary progesterone. However, women who spent their childhood in Sylhet have a lower proportion of ovulatory cycles compared to women who developed in Britain. These group differences in ovulation frequency indicate more qualitative effects of contrasting developmental environments. We discuss possible explanations for differences in response between progesterone and estradiol, as well as broader implications of our findings.

Early puberty is a risk factor for adult diseases and biomedical and psychosocial research implicate growth (in height and weight) and stress as modifiable drivers of early puberty. Seldom have studies examined these drivers simultaneously or concurrently using quantitative and qualitative methods. Within the context of migration, we used mixed-methods to compare growth, stress and puberty in a study of 488 girls, aged 5–16, who were either Bangladeshi, first-generation migrant to the UK, second-generation migrant, or white British (conducted between 2009 and 2011). Using a biocultural framework, we asked the questions: 1) Does migration accelerate pubertal processes? 2) What biocultural markers are associated with migration? 3) What biocultural markers are associated with puberty? Girls self-reported pubertal stage, recalled 24-h dietary intake, and answered questions relating to dress, food, and ethnic identity. We collected anthropometrics and assayed saliva specimens for dehydroepiandrosterone-sulfate (DHEA-S) to assess adrenarcheal status. Our findings demonstrate that first-generation migrants had earlier puberty than second-generation migrants and Bangladeshi girls. British style of dress did not increase with migration, while dietary choices did, which were reflected in increasing body mass index. However, the widely-used phrase, “I'm proud of my religion, but not my culture” demonstrated that ethnic identity was aligned more with Islamic religion than ‘Bangladeshi culture.’ This was epitomized by wearing the hijab, but denial of eating rice. The social correlates of puberty, such as ‘practicing’ wearing the hijab and becoming ‘dedicated to the scarf,’ occurred at the same ages as adrenarche and menarche, respectively, among first-generation girls. We suggest that the rejection of ‘Bangladeshi culture’ might be a source of psychosocial stress for first-generation girls, and this may explain elevated DHEA-S levels and early puberty compared to their second-generation counterparts. Our results support a biocultural model of adolescence, a period for biological embedding of culture, when biological and psychosocial factors adjust developmental timing with potential positive and negative implications for long-term health.

Timing of breast development (or thelarche) and its endogenous and exogenous determinants may underlie global variation in breast cancer incidence. The study objectives were to characterize endogenous estrogen levels and bisphenol A (BPA) exposure using a migrant study of adolescent girls and test whether concentrations explained differences in thelarche by birthplace and growth environment. Estrogen metabolites (EM) and BPA-glucuronide (BPA-G) were quantified in urine spot samples using liquid chromatography tandem mass spectrometry (LC-MS/MS) from a cross-sectional study of Bangladeshi, first- and second-generation Bangladeshi migrants to the UK, and white British girls aged 5–16 years (n = 348). Thelarche status at the time of interview was self-reported and defined equivalent to Tanner Stage ≥2. We compared geometric means (and 95% confidence interval (CIs)) of EM and BPA-G using linear regression and assessed whether EM and BPA-G explained any of the association between exposure to the UK and the age at thelarche using hazard ratios and 95% confidence intervals. Average EM decreased with exposure to the UK, whereas BPA-G increased and was significantly higher among white British (0.007 ng/mL, 95% CI: 0.0024–0.0217) and second-generation British-Bangladeshi girls (0.009 ng/mL, 95% CI: 0.0040–0.0187) compared to Bangladeshi girls (0.002 ng/mL, 95% CI: 0.0018–0.0034). Two of four EM ratios (16-pathway/parent and parent/all pathways) were significantly associated with thelarche. The relationship between exposure to the UK and thelarche did not change appreciably after adding EM and BPA-G to the models. While BPA-G is often considered a ubiquitous exposure, our findings suggest it can vary based on birthplace and growth environment, with increasing levels for girls who were born in or moved to the UK. Our study did not provide statistically significant evidence that BPA-G or EM concentrations explained earlier thelarche among girls who were born or raised in the UK.