- (1) To review research on catch-up growth after chronic undernutrition.
- (2) To review the relationship between catch-up growth and early pubertal development.
2. Fetal Undernutrition in Relation to Later Growth and Puberty
- - Lack of nutrients due to deficient maternal nutrition. This is the major cause in the developing world.
- - Placental defects.
- - Fetal disease
- - Maternal disease
2.1. Catch-Up Growth
2.2. Pubertal Development
- - Infants born into a resource-poor environment may not undergo catch-up growth due to nutrient deficiency and diseases, particularly infections.
- - Postnatal catch-up growth is possible under favourable conditions for the majority of undernourished infants born SGA.
- - Prenatal growth restriction followed by postnatal catch-up growth may be associated with earlier timing of puberty.
- - Girls born SGA and children born preterm with VLBW are prone to early pubertal development.
3. Postnatal Undernutrition, Growth and Puberty
3.1. Gastrointestinal Disease
3.1.1. Crohn’s Disease
3.1.2. Celiac Disease
3.3. Eating Disorders
3.4. Early Postnatal Undernutrition and Critical Periods
- - Well-nourished children may become undernourished due to inadequate diet or disease. Their growth may be retarded and puberty delayed.
- - After successful treatment, catch-up growth can occur, but may be prolonged. There are conflicting reports regarding whether full catch-up is possible.
- - There may be critical periods for the potential for catch-up growth.
- - To the best of our knowledge, catch–up growth in children, following undernutrition which occurs only postnatally, has not been reported to be associated with earlier pubertal development.
4. Combined Fetal-Postnatal Undernutrition, Growth and Puberty
4.1. Catch-Up Growth
4.2. Pubertal Development
- - Children who have been undernourished in utero and continue life in an environment where food is scarce, will not experience catch-up growth. They will enter puberty later than a well-nourished reference population.
- - On the other hand, chronically undernourished children who are transferred to an environment with abundant food supply will undergo catch-up growth of varying degrees, and may develop early puberty.
- - The timing for the onset of puberty is dependent on the degree of undernutrition as well as the rate of catch up growth.
- - Prepubertal adopted children have been reported to have elevated gonadotropins.
5. General Discussion
5.1. Metabolic Signalling, Nutritional Supply and the Onset of Puberty
5.2. Endocrine Disruptors and Early Pubertal Development
5.3. Catch-Up Growth and Pubertal Development
- - Early puberty may occur following catch-up growth after fetal or fetal-postnatal undernutrition, i.e., chronic undernutrition starting already during intrauterine life [29,71,72]. To the best of our knowledge, early puberty has not been reported after catch-up growth following isolated postnatal undernutrition in humans.
- - The timing of pubertal development may be preprogrammed during early life. In a study of girls adopted from India, menarche occurred at similar height and weight as in a reference population of underprivileged girls in India. The adopted girls had a mean age at menarche of 11.8 years, compared with 14.4 years in the underprivileged group [71,72]. This may indicate a programming not linked to chronological age but to the attainment of a degree of biological maturation parallelled by a certain height and weight.
- - Several groups have reported a close connection between growth acceleration and the rate of pubertal development [69,71,72,73,77,110,111,112] In a study of girls adopted from India, Proos et al.  demonstrated that the more pronounced the degree of stunting and the faster the catch-up growth, the earlier menarche ocurred. Papadimitriou et al. [111,112] have suggested that growth acceleration up to 2–4 years of age, is a predictor both of early pubertal development and of obesity. The authors also point out that the catch-up growth occurring after intrauterine growth retardation and that of adopted children could possibly represent similar processes.
- - Tam et al.  studied the influence of prenatal and postnatal growth on the timing of menarche, and found that it occurred earlier in girls who were long and light at birth and who had higher fat mass and circulating IGF-I during childhood. Age at menarche was best predicted by combining size at birth and BMI z-score at 8 years of age.
- - In order to create a situation analogous to that of undernutrition in internationally adopted children, Bourguignon et al.  studied the effect of varying the early nutritional conditions in the rat. The authors showed that rats subjected to restricted feeding had delayed hypothalamic and testicular maturation as compared to rats having access to more food. If food-restricted rats were allowed to refeed after nutritional deprivation the growth rate increased. This was associated with accelerated testicular and hypothalamic maturation. However, the effect was only observed when refeeding occurred before weaning. The findings indicate that hypothalamic maturation is influenced by variations in nutritional status and growth rate during a critical period. In addition, there was an acceleration of maturation of the glutamate receptor-dependent secretion of GnRH, suggesting the involvement of hypothalamic glutamate receptors. This is another significant paper, indicating lines of experimental research that may help in clarifying the reasons behind early pubertal development after catch-up following undernutrition.
- - The importance of dietary energy for LH-pulsatility has been also been pointed out by Loucks  in a study on adolescent and young adult women.
- - Foster and Olster  have reported that gonadotropins were elevated during catch-up growth in lambs. They found that severe undernutrition prevented ovulation by impairing the system governing GnRH secretion and its production of high-frequency LH pulses. Ad libitum feeding of growth-retarded lambs resulted in rapid catch-up growth, a progressive several-fold increase in LH pulse frequency and onset of reproductive cycles. The data are important, since the results are analogous to those reported for undernourished children. Moreover, it links the occurrence of catch-up growth to the simultaneous increase of LH-pulse frequency.
- - As stated above, elevated gonadotropins were found in prepubertal adopted girls in a Danish study .
Thus, the following sequence of events seems reasonably well documented: Nutritional rehabilitation after persistent undernutrition leads to catch-up growth, coinciding with increased gonadotropin secretion, eventually leading to early puberty.
- Following nutritional rehabilitation catch-up growth is possible after fetal, postnatal and combined fetal-postnatal undernutrition.
- Studies on adopted children arriving in their new environment at various ages show that catch-up growth can take place at any time during childhood but may be limited by critical periods.
- Early/precocious puberty following catch-up growth after fetal or fetal-postnatal undernutrition has been reported in a number of studies.
- Early pubertal development does not seem to follow catch-up growth after isolated postnatal undernutrition.
- The timing for the onset of puberty is dependent on the degree of undernutrition as well as the rate of the catch-up growth.
- Experiments in sheep have shown that catch-up growth after undernutrition is associated with an increased frequency of LH-pulses,
- Gonadotropins have been found to be elevated in adopted girls, who are still prepubertal.
Conflict of interest
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