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CHAPTER 18 Nutrition and Reproduction CHAPTER 18 Nutrition and Reproduction Nanette Santoro Alex J. Polotsky Jessica Rieder Laxmi A. Kondapalli In males, pulsatile gonadotropin-releasing hormone (GnRH) characterized molecule to date is leptin. It has been shown and gonadotropin secretion occurs at a mean interval of in both animal models10 and in humans that inadequate leptin every 2 hours,1 a frequency sufficient to maintain testosterone is associated with lack of GnRH secretion, and that leptin secretion, normal virilization, and spermatogenesis. In females, replacement can restore normal cycles in women who have a more complex series of gonadal tasks must be accomplished, hypothalamic amenorrhea and hypoleptinemia.11 However, which include maturation of a single follicle, follicular rupture leptin alone is insufficient to initiate pubertal maturation of and ovulation, and corpus luteum formation. The mature the hypothalamic-pituitary-gonadal (HPG) axis and a specific female hypothalamic-pituitary-ovarian (HPO) axis must leptin concentration or threshold, above which maturation respond dynamically with negative and then positive (bimodal) occurs, has not been identified.12 feedback to rising estradiol, which is secreted by the develop- One of the final common pathways that appears to activate ing follicle.2 The positive feedback response, in the form of GnRH-LH secretion during puberty involves kisspeptin a luteinizing hormone (LH) surge, must be sufficient to and its cognate receptor, G-protein coupled receptor-54 initiate the molecular events of follicle rupture and subsequent (GPR54).13 Kisspeptin appears to act directly on GnRH luteinization. Optimal functioning of the female reproductive neurons and amplifies GnRH and consequently LH and system requires more versatility of the HPO axis, and this follicle-stimulating hormone (FSH) secretion. Both kisspeptin system is therefore more vulnerable to disruption than is and its receptor, GPR54, increase coincident with the onset the male (see Chapters 1, 12, and 20).3 of puberty. In addition to kisspeptin, there are many other Pulsatile secretion of hypothalamic GnRH and pituitary LH upstream regulators of GnRH that appear to provide redun- occurs prior to birth and continues throughout the prepubertal dancy to prevent reproductive failure. period.4 Pulsatile LH secretion has been detected in children Puberty is also a time during which acquisition of functional and occurs at a normal, adult frequency in boys and girls5; networks of neurons and glial cells provide necessary com- however, the amplitude of the signal is miniscule and requires munication pathways through which reproductive signaling highly sensitive measurement methods to detect. Suppression can occur. The acquisition of these networks may involve of pulsatile GnRH-LH secretory amplitude in prepuberty anatomic changes in cell populations or recruitment as well has been attributed to a combination of enhanced sensitivity as increases in neuronal connectivity. For example, glial cells of the childhood reproductive axis to estradiol, as well as long believed to be inert but helpful in providing scaffolding a predominance of inhibitory neural and neuroendocrine may play a more direct role in GnRH secretion. Microglia, signals that ultimately dampen the amplitude of the central macrophages that differentiate into glial cells, are necessary GnRH pulse generator.6 This working model hypothesizes that for optimal GnRH secretion. Colony-stimulating factor prepubertally, the HP axis is inhibited, and during puberty (CSF)-1 knockout mice, which lack adequate macrophage the axis is released from this inhibition. function, do not have adequate microglial development and Over 40 years ago, Frisch and Revelle noted a direct are deficient in hypothalamic GnRH secretion.14 The interac- relationship between body weight and age at onset of tion of immunomodulatory molecules with the reproductive puberty7,8 and concluded that a critical amount of body fat neural networking is not yet well characterized. was needed for the onset of puberty (see Chapter 17).9 Much research to date on abnormalities of pubertal matura- These investigators predicted correctly that adipose tissue tion has focused on inadequate nutritional states. However, in somehow provided a permissive signal to the reproductive the United States as in most developed nations, these condi- system. The discovery of the endocrine nature of adipose tions are becoming increasingly rare and are being replaced tissue has since led to the identification of a number of by reproductive dysfunction due to overweight and obesity. adipokines as well as inflammatory factors, and the elucidation Obesity has been linked to altered pubertal progression and of their role in reproduction is emerging rapidly. The best adult reproductive dysfunction. Polycystic ovary syndrome 447 CHAPTER 18 Nutrition and Reproduction 447.e1 Abstract There appears to a be an optimal window of nutritional sufficiency to allow for reproduction to occur in males and females. The male hypothalamic pituitary (HP) axis is rela- tively static and therefore is more resistant to nutritional perturbations than is the female HP axis. However, accumulat- ing data indicate that both under- and overnutrition have consequences on the pace of sexual maturation in humans and on subsequent reproductive function. This chapter will review current knowledge of this field. Keywords Puberty hypothalamus pituitary obesity nutrition 448 PART 2 Pathophysiology and Therapy: Pediatric, Adolescent, and Adult (PCOS) has been well studied in its interactions between majority of girls after the 20th menstrual period. However, obesity and anovulation; however, a far greater proportion even weekly urine sampling may be inadequate for the of the population is affected by simple obesity. Pubertal detection of brief excursions of progesterone, or its urinary onset is earlier in obese girls and boys, but the tempo of metabolite, pregnanediol glucuronide (PDG). Luteal phases puberty is slowed in simple obesity.15,16 A relative state of may also be shorter than the adult norm of 14 days when hypogonadotropic hypogonadism has been described in obese adolescents are observed. Data from our group indicates that women without PCOS.17 Decreased fecundity, increased the capacity to produce an ovulatory LH surge in response reproductive wastage, and a less favorable response to fertility to estrogen is present even before the onset of the first treatments have all been described in association with adult menses.32 These findings indicate that, at least in some girls, female obesity.18-21 In men, reduced fertility and a marked a biphasic feedback response to estradiol is not the rate increase in bioavailable estrogen have been described.22,23 limiting step in attaining regular, ovulatory menses. Irregular This chapter discusses the role of overnutrition and menstruation has been associated with low gynecologic age, undernutrition in relation to reproduction and provides low body mass index (BMI), chronic nonspecific lung disease emerging data from clinical trials designed to ameliorate the or allergic disease, weight loss, and stress.34 adverse effects of obesity on puberty and adult reproductive Rosenfield has hypothesized that low-amplitude hormonal function. cycles occur in early puberty, with nighttime levels greater than daytime. Indeed, it may be that all the hormonal Nutrition and Puberty components of the HPO axis are functioning at an adult frequency, but the hormonal signals are dampened and slowly ◆ Initiation of puberty likely represents a release from chronic increase to detectable levels.35 inhibition of the HPG axis in both boys and girls. Prior epidemiologic studies documenting the age of attain- ◆ Low-amplitude hormone fluctuations may occur during the ment of regular menstruation were conducted in populations prepubertal period. of girls who differ from our modern-day US population. ◆ Obesity may affect the timing of puberty by advancing its There were few young women of color, yet African-American onset, but it may slow the tempo and have an inconsistent girls are known to attain menarche and to undergo pubertal effect on the timing of menarche. maturation earlier than Caucasian girls. This has been related ◆ The known and conjectured mechanisms initiating puberty in part to increased BMI but may also be due to other are reviewed elsewhere in this volume. We will focus on the factors.36 It is possible that prior populations studied have relevant epidemiology of normal puberty in boys and girls. been enriched in girls who were nutritionally marginal, certainly so by today’s standards. However, weight or BMI Puberty appears to be imminent when hypothalamic- data are not available from these earlier studies.29,37,38 Given pituitary sensitivity to negative feedback inhibition by estradiol the high rates of obesity among adolescents in the current is reduced,24 and attendant inhibitory neural networks diminish US population, and the increase in body fat in adolescent in activity. These processes lead to increased GnRH secre- women in the United States over the past century,39 it is tion25 as well as increased gonadotropin pulsatility, initially likely that any restraint that low body weight might place at nighttime, which then extends throughout 24 hours.26 upon the HPO axis is minimally operative in our current The result is folliculogenesis in girls, spermatogenesis and society.40 The virtual elimination of undernutrition might be testosterone production in boys, and
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