Human reproduction and health: an evolutionary perspective Supplementary online material G. Jasienska, R. G. Bribiescas, A.-‐S. Furberg, S. Helle, A. Núñez-‐de la Mora The Lancet 390: 510-‐520, 2017 If you would like a pdf of full text of this article, please send email at
[email protected] Table 1. Summary of evidence linking prenatal and postnatal nutritional and energetic conditions on reproductive function FACTOR
REPRODUCTIVE TRAIT
Ref
KEY FINDING
Evidence linking infancy and childhood diet with reproductive function Diet
Puberty
Diet
Puberty
Diet
Puberty
Diet
Menarche
Diet
Menopause
Infant diet
Menarche
Infant diet
Ovarian function
Children with higher vegetable intake reached puberty later than average whereas those with higher animal protein intake reached puberty earlier than average Children with lower diet quality pre-‐puberty, experience pubertal growth spurt at an earlier age than children with a higher diet quality Protein intake from dairy but not animal meat, particularly at age 5–6 years, is associated with earlier indices of puberty (e.g. pubertal growth spurt, menarche, voice break), independently of BMI. Increased milk intake from 5 to 12 years of age was weakly associated with earlier menarche High consumption of carbohydrate vegetable, fibre and cereal products were inversely related to age at menopause; Women with higher intake of total fat, protein and meat experienced a delayed onset of menopause. Longer duration of exclusive breast feeding was associated with later onset of menarche Formula feeding, independently of infant size, was associated with higher oestradiol levels in boys and girls and with higher testosterone in girls
1
2
3
4 5
6 7
Reviews: 8-10
Evidence linking prenatal growth and reproductive function Small for gestational age (SGA)* Small for gestational age (SGA) Small for gestational age (SGA)
Gynaecological characteristics Ovarian development
Small for gestational age (SGA)
Ovarian function
Small for gestational age
Ovarian reserve
Ovulation
Adolescent women born SGA were shown to have reduced uterine and ovarian volume SGA infants had reduced primordial follicle number compared with gestationally matched appropriately grown infants Prevalence of anovulation in adolescent girls was higher among SGA than in matched appropriate for gestational age (AGA)** group SGA infants exhibited hypersecretion of follicle-‐stimulating hormone (FSH) in early infancy, and girls who were born SGA also during early post-‐menarche. No significant reduction in indicators of ovarian reserve in
11,12 12,13 14
15,16
17,18
(SGA) and low birth weight (LBW)*** Small for gestational age (SGA)
Small for gestational age (SGA)
adolescent girls and young women born SGA or LBW controlling for gestational age. Puberty and menarche
Testicular function
Low birth weight (LBW)
Ovarian function
Low birth weight (LBW)
Menarche and adult body height Pubertal growth
Very low birth weight (VLBW) Ponderal index
Ovarian function
Birth size
Gonadal function
In girls born SGA, the age at pubertal onset and the age at menarche were advanced by about 5–10 months compared to girls born appropriate for gestational age. There was no corresponding difference for boys. Age at onset of puberty was significantly lower in persistently short SGA children as compared to short children born appropriate for gestational age (AGA). Menarche was advanced in girls born SGA. Adult males born SGA exhibited elevated levels of oestradiol, dihydrotestosterone and inhibin B. Post-‐pubertal males born SGA had reduced testicular volume, lower testosterone and higher LH levels Female infants with low birth weight had an exaggerated response to GnRH and increased ovarian production of anti-‐Mullerian hormone (AMH) compared with appropriately grown infants Girls with low birth weight experienced a faster progression to an early menarche and to a reduced adult height The pubertal growth spurt occurred significantly earlier in preterm VLBW individuals than in controls born at term, regardless of whether they were born SGA or AGA Ponderal index at birth (indicator of neonatal nutritional status) was positively associated with concentrations of 17b oestradiol during adulthood Women with low ponderal index show greater sensitivity to energetic stress in adulthood. Taller maternal height and larger birth size were associated with lower oestradiol levels in girls and higher testosterone levels in boys infants
19-21 22 23 24 25
BUT SEE:
26 27
28,29 30
31 32 7
Reviews: 33 * SGA -‐ small for gestational age: infants whose birth weight is < the 10th percentile for gestational age ** AGA -‐ appropriate for gestational age: infants whose size is within the normal range for his or her gestational age *** LBW -‐ low birth weight: infants whose birth weight is less than 2,500 g regardless of gestational age Evidence linking postnatal growth and reproductive function
Body weight
Puberty
Body weight Body weight
Menarche Menopause
Weight gain Weight gain
PCOS (Polycystic ovary syndrome) Menopause
Weight gain
Reproductive strategy
Excessive weight gain
Puberty
Nutritional supplementation
Age at menarche
BMI at 7 years of age was inversely correlated with the start and peak of a child’s growth spurt as indicators of puberty timing Girls with high BMI were at higher risk of early menarche Duration of lactation and weight at 2 years of age were positively related to age at menopause Higher risk of PCOS for women born SGA followed by catch-‐up weight gain Low weight gain in infancy, rather than low birth weight, is associated with earlier menopause Males with rapid weight gain from birth to 6 months of age reached puberty earlier and, as young adults, had higher testosterone levels, were taller, more muscular, had higher grip strength, and were more sexually active Excessive increase in BMI between the ages of 2 and 8 years was related to an advancement of puberty, and ultimately a loss in adolescent height gain. No relationship between nutritional supplementation during childhood and age at menarche. Year of birth and socioeconomic status were negatively associated with age at menarche suggesting an effect of early life conditions on reproductive maturation.
34 35 36 37,38 39,40 41
42
43
Evidence on the association between prenatal growth, postnatal growth and reproductive function Prenatal and postnatal interactions
Adrenarche
Prenatal and postnatal interactions
Puberty
Prenatal and postnatal interactions
Menarche
Prenatal and postnatal interactions
Ovarian function
Girls small at birth, who experienced catch-‐up growth with a BMI higher in childhood than at birth, were at risk of an earlier adrenarche, as manifested by increased dehydroepiandrosterone sulphate (DHEAS) secretion Adrenal androgen concentrations were highest in those small infants who become heavier than average during early childhood A relatively low body weight and rapid weight gain between birth and 24 months were independently associated with an earlier age in onset of puberty Girls who were relatively long and thin at birth (>49 cm,
