Childhood Conditions Influence Adult Progesterone Levels

Abstract

Background

Average 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 Findings

To 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).

Conclusions

This 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.

Abstract

Alejandra Núñez-de la Mora and colleagues found that women of Bangladeshi origin who had spent their childhood in the UK had higher progesterone levels and matured earlier than those who had been children in Bangladesh.

Editors' Summary

Background.

Women's reproductive biology—which includes levels of sex hormones at different stages of the menstrual cycle—is known to vary greatly depending on the environment. This variation can be measured by looking at the levels of certain reproductive hormones in the saliva, for example, progesterone and estradiol. The levels of these hormones differ greatly from individual to individual. Women who live in environments where less food is available or infections are more common, or who do more physical work seem to have lower levels of these hormones compared to other women. Because these differences seem to persist over the long term, some researchers have suggested that various factors relating to an individual's environment early in life have a strong influence on later fertility. This theory is based on ideas drawn from evolutionary biology and ecology. Theoretically, a woman who limits her future fertility as a biological response to poor environments would eventually have greater evolutionary success than an individual who remains fertile in harsh conditions. Although the logical basis for this idea is attractive, there is not very much evidence that it is true.

Why Was This Study Done?

In this study, the researchers wanted to collect experimental evidence from human populations that would help them test the hypothesis outlined above. The study performed here made use of a “natural experiment” resulting from widespread migration of people from Bangladesh to the UK. 95% of these individuals come from one particular region of Bangladesh, Sylhet. People would experience extensive differences between the environments before and after migration, including economic factors, access to health services, exposure to infectious diseases, and so on. Therefore, a comparison of hormone levels between individuals who had migrated at different periods during their life might help to test the theory that early environmental factors affect later fertility.

What Did the Researchers Do and Find?

Five groups of women were selected and compared in this study. The groups included women who had grown up in Bangladesh but moved to the UK as adults; women who were born in Bangladesh but moved to the UK as children; women whose parents were from Bangladesh but who were born and raised in the UK; Bangladeshi women who were born and raised in Bangladesh; and finally a comparison group of women of European descent who were born and raised in the UK. Each woman in each of the five groups was asked to collect a sample of her own saliva each day for one menstrual cycle. The researchers tested the saliva samples to find out the levels of progesterone. The average progesterone level for the last 14 days of each woman's menstrual cycle (when progesterone levels are generally high) was then calculated and these values compared across the five groups. In particular, the researchers looked at the relationship between the age at which an individual arrived in the UK, the time spent in the UK, and the progesterone levels in saliva.

The researchers found statistically significant differences in progesterone levels between individuals who had migrated as children, second-generation migrants, and women of European descent, as compared to the levels for Bangladeshi women who had never migrated and women who migrated as adults. Progesterone levels for the first three groups were higher than those for the Bangladeshi women who had not migrated or who had migrated as adults. The age at which women migrated also seemed to be linked to their progesterone levels. Amongst women who migrated before the start of menstruation, those who migrated at a younger age had higher average progesterone levels. However, this relationship did not seem to hold true for women who had migrated after they started menstruating.

What Do These Findings Mean?

This study suggests that certain indicators of reproductive biology, such as progesterone levels, may be linked to environmental factors that an individual experiences early in life. The findings support the idea that harsh environments early in development are associated with lower fertility later in life. However, it is not clear from this study which precise environmental factors are involved; it is possible that exposure to infectious disease is important, but this possibility was not specifically tested in this research study. Finally, it is not certain whether the lower average progesterone levels of the particular groups studied would actually translate into lower fertility. It is possible that although certain individuals and groups had lower levels of this hormone, they may in fact have been as fertile as individuals with higher levels of the hormone.

Additional Information.

Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.0040167.

• Information from the US National Institutes of Health on fertility and infertility

• Wikipedia entry on progesterone (Wikipedia is an internet encyclopedia anyone can edit)

• Resources from the World Health Organization about sexual and reproductive health, including links to resources on family planning, infertility, and other related topics

• World Health Organization country site for Bangladesh, providing key statistics and health resources

• Moving Here: stories and experiences told of individuals' emigration to the UK