Undernutrition during fetal and postnatal life is still a major problem in many low- and middle-income countries. Even in high-income countries malnutrition may exist in cases of intrauterine growth retardation, as well as in chronic conditions such as anorexia nervosa and inflammatory bowel disease. Children adopted from developing countries are often chronically malnourished. Nutritional rehabilitation, resulting in catch-up growth, is often complicated by influences originating in fetal life as well as during postnatal growth. This may result in hormonal and metabolic changes as well as alterations in pubertal development. The present review focuses on fetal, postnatal and fetal-postnatal undernutrition and subsequent catch-up growth as well as catch-up growth in relation to pubertal development. Catch-up growth in children can be associated with early puberty following fetal or combined fetal-postnatal undernutrition. However, early puberty does not seem to occur following catch-up growth after isolated postnatal undernutrition. Gonadotropins have been reported to be elevated in prepubertal adopted girls as well as during catch-up growth in animals. Even if other factors may contribute, linear catch-up growth seems to be associated with the timing of pubertal development. The mechanisms behind this are still unknown. Future research may elucidate how to carry out nutritional rehabilitation without risk for early pubertal development.
References
[1]
De Onis, M.; Garza, C.; Onyango, A.W.; Rolland-Cachera, M.F. le Comité de nutrition de la Societé francaise de pédiatrie. WHO growth standards for infants and young children. Arch. Pediatr. 2009, 16, 47–53.
[2]
Measuring change in nutritional status. Guidelines for Measuring the Impact of Supplementary Feeding Programmes for Vulnerable Groups; World Health Organisation: Geneva, Switzerland, 1983.
[3]
Waterlow, J.C.; Buzina, R.; Keller, W.; Lane, J.M.; Nichaman, M.Z.; Tanner, J.M. The presentation and use of height and weight data for comparing the nutritional status of groups of children under the age of 10 years. Bull. World Health Organ. 1977, 55, 489–498.
[4]
Karlberg, J.; Kwan, C.W.; Albertsson-Wikland, K. Reference values for change in body mass index birth to 18 years of age. Acta Paediatr. 2003, 92, 648–652, doi:10.1111/j.1651-2227.2003.tb00593.x.
[5]
Prader, A. Catch-up growth. Postgrad. Med. J. 1978, 54, S133–S146.
[6]
Prader, A.; Tanner, J.M.; von Harnack, G.A. Catch-up growth following illness or starvation. An example of developmental canalisation in man. J. Pediatr. 1963, 62, 646–681, doi:10.1016/S0022-3476(63)80035-9.
Hornick, J.L.; van Eanaeme, C.; Gérard, O.; Dufrasne, I.; Istasse, L. Mechanisms of reduced and compensatory growth. Domest. Anim. Endocrinol. 2000, 19, 121–132, doi:10.1016/S0739-7240(00)00072-2.
[9]
Wit, J.M.; Boersma, B. Catch-up growth: Definitions, mechanisms and models. J. Pediatr. Endocrinol. Metab. 2002, 15, S1229–S1241.
[10]
Golden, M.H. Is complete catch-up possible for stunted malnourished children? Eur. J. Clin. Nutr. 1994, 48, S58–S70. discussion S71.
[11]
Saxena, A.; Phadke, S.R.; Agarwal, S.S. Linear catch-up growth. Indian J. Pediatr. 2000, 67, 225–230.
[12]
UNICEF. State of the World’s Children 2009; UNICEF: New York, NY, USA, 2009.
[13]
Saxena, N.; Nayar, D.; Kapil, U. Prevalence of underweight, stunting and wasting. Indian Pediatr. 1997, 34, 627–631.
[14]
Adair, L.S. Developing World Perspective: The Importance of Growth for Short-Term Health. In Importance of Growth for Health and Development; Lucas, A., Makrides, M., Ziegler, E.E., Eds.; Nestlé Nutr. Inst. Workshop Ser. Pediatr. Program: Basel, Switzerland, 2011; Volume 65, pp. 71–83.
[15]
Pelletier, D.L.; Frongillo, E.A., Jr.; Schroeder, D.G.; Habicht, J.P. The effects of malnutrition on child mortality in developing countries. Bull. World Health Organ. 1995, 73, 443–448.
[16]
Godfrey, K.M.; Barker, D.J. Fetal nutrition and adult disease. Am. J. Clin. Nutr. 2000, 71, 13444S–13452S.
[17]
Barker, D.J.P.; Osmond, C.; Kajantie, E.; Eriksson, J.G. Growth and chronic disease: Findings in the Helsinki Birth Cohort. Ann. Hum. Biol. 2009, 26, 445–458.
[18]
Barker, D.J. In utero programming of chronic disease. Clin. Sci. (Lond.) 1998, 95, 115–128, doi:10.1042/CS19980019.
[19]
Delisle, H. Foetal programming of nutrition-related chronic diseases. Santé 2002, 12, 56–63.
[20]
Lucas, A. Growth and later health: A general perspective. Nestlé Nutr. Workshop Ser. Pediatr. Program. 2010, 65, 1–9. discussion 9–11., doi:10.1159/000281107.
[21]
Popkin, B.M. Global changes in diet and activity patterns as drivers of the nutrition transition. Nestlé Nutr. Inst. Workshop Ser. Pediatr. Program. 2009, 63, 1–14, doi:10.1159/000209967.
Bhargava, S.K.; Sachdev, H.S.; Fall, C.H.; Osmond, C.; Lakshmy, R.; Barker, D.J.; Biswas, S.K.; Ramji, S.; Prabhakaran, D.; Reddy, K.S. Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthood. N. Engl. J. Med. 2004, 350, 865–875.
Creasy, R.K.; Resnik, R. Intrauterine Growth Restriction. In Maternal—Fetal Medicine, 4th; Creasy, R.K., Resnik, R., Eds.; Saunders: Philadelphia, PA, USA, 1999; pp. 569–584.
[26]
Niklasson, A.; Ericson, A.; Fryer, J.G.; Karlberg, J.; Lawrence, C.; Karlberg, P. An update of the Swedish reference standards for weight, length and head circumference at birth for a given gestational age (1977–1981). Acta Paediatr. Scand. 1991, 80, 756–762.
[27]
Albertsson-Wikland, K.; Karlberg, J. Natural growth in children born small for gestational age with and without catch-up growth. Acta Paediatr. 1994, Suppl. 399, 64–70, doi:10.1111/j.1651-2227.1994.tb13292.x.
[28]
Albertsson-Wikland, K.; Wennergren, G.; Wennergren, M.; Vilbergsson, G.; Rosberg, S. Longitudinal follow-up of growth in children born small for gestational age. Acta Paediatr. 1993, 82, 438–443, doi:10.1111/j.1651-2227.1993.tb12718.x.
[29]
Persson, I.; Ahlsson, F.; Ewald, U.; Tuvemo, T.; Qingyuan, M.; von Rosen, D.; Proos, L. Influence of perinatal factors on the onset of puberty in boys and girls. Implications for interpretation of link with risk of long term diseases. Am. J. Epidemiol. 1999, 150, 747–755, doi:10.1093/oxfordjournals.aje.a010077.
[30]
Lazar, L.; Pollak, U.; Kalter-Leibovici, O.; Pertzela, A.; Phillip, M. Pubertal course of persistently short children born small for gestational age (SGA) compared with idiopathic short children born appropriate for gestational age (AGA). Eur. J. Endocrinol. 2003, 149, 425–432, doi:10.1530/eje.0.1490425.
[31]
Ibanez, L.; de Zegher, F. Puberty and prenatal growth. Mol. Cell. Endocrinol. 2006, 154, 22–25, doi:10.1016/j.mce.2006.04.010.
[32]
Ibanez, L.; de Zegher, F. Puberty after prenatal growth restraint. Horm. Res. 2006, 65, S112–S115, doi:10.1159/000091515.
[33]
Ibanez, L.; Ferrer, A.; Marcos, M.V.; Hierro, F.R.; de Zegher, F. Early puberty: Rapid progression and reduced final height in girls with low birth weight. Pediatrics 2000, 106, E72–E74.
[34]
Ibanez, L.; Jimenez, R.; de Zegher, F. Early puberty-menarche after precocious pubarche: Relation to prenatal growth. Pediatrics 2006, 117, 117–121.
[35]
Ibanez, L.; Potau, N.; Francois, I.; de Zegher, F. Precocious pubarche, hyperinsulinism and ovarian hyperandrogenism in girls: Relation to reduced fetal growth. J. Clin. Endocrinol. Metab. 1998, 83, 3558–3662, doi:10.1210/jc.83.10.3558.
[36]
Dunger, D.B.; Ahmed, M.L.; Ong, K.K. Early and late weight gain and the timing of puberty. Mol. Cell. Endocrinol. 2006, 254-255, 140–145, doi:10.1016/j.mce.2006.04.003.
[37]
Davison, K.K.; Susman, E.J.; Birch, L.L. Percent body fat at age 5 predicts earlier pubertal development among girls at age 9. Pediatrics 2003, 111, 815–821, doi:10.1542/peds.111.4.815.
[38]
Rolland-Cachera, M.F.; Deheeger, M.; Maillot, M.; Bellisle, F. Early adiposity rebound: Causes and consequences for obesity in children and adults. Int. J. Obes. 2006, 30, S11–S17, doi:10.1038/sj.ijo.0803514.
[39]
Williams, S.; Dickson, N. Early growth, menarche, and adiposity rebound. Lancet 2002, 359, 580–581, doi:10.1016/S0140-6736(02)07715-2.
[40]
Engelbregt, M.J.; Houdijk, M.E.; Popp-Snijders, C.; Delmarre-van de Waal, H.A. The effect of intra-uterine growth retardation and postnatal undernnutrition on onset of puberty in male and female rats. Pediatr. Res. 2000, 48, 803–807, doi:10.1203/00006450-200012000-00017.
[41]
Léonhardt, M.; Lesage, J.; Croix, D.; Dutriez-Casteloot, I.; Beauvillain, J.C.; Dupouy, J.P. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of pubrty. Biol. Reprod. 2003, 68, 390–400.
[42]
Woelfle, J. Postnatal consequences of intrauterine development: Pubertal development in children born small for gestational age. Klin. P？diatr. 2008, 220, 10–15, doi:10.1055/s-2007-971046.
[43]
Wehkalampi, K.; Hovi, P.; Dunkel, L.; Strang-Karlsson, S.; J？rvenp？？, A.L.; Eriksson, J.G.; Andersson, S.; Kajantie, E. Advanced pubertal growth spurt in subjects born preterm: The Helsinki study of very low birth weight adults. J. Clin. Endocrinol. Metab. 2011, 96, 525–533.
[44]
Simon, D. Puberty in chronically diseased patients. Horm. Res. 2002, 57, S53–S56, doi:10.1159/000058102.
[45]
Griffits, A.M. Growth retardation in early-onset inflammatory bowel disease: Should we monitor and treat these patients differently? Dig. Dis. 2009, 27, 404–411, doi:10.1159/000228581.
[46]
Bosio, L.; Barbera, G.; Mistura, L.; Sassi, G.; Bianchi, C. Growth acceleration and final height after treatment for delayed diagnosis of celiac disease. J. Pediatr. Gastroenterol. Nutr. 1990, 11, 324–329, doi:10.1097/00005176-199010000-00007.
[47]
Wolthers, O.D. Growth problems in children with asthma. Horm. Res. 2002, 57, 83–87, doi:10.1159/000058107.
[48]
Swenne, I. Weight requirements for catch-up growth in girls with eating disorders and onset of weight loss before menarche. Int. J. Eat. Disord. 2005, 38, 340–345, doi:10.1002/eat.20182.
[49]
Lantzouni, E.; Frank, G.R.; Golden, N.H.; Shenker, R.I. Reversibility of growth stunting in early onset anorexia nervosa: A prospective study. J. Adolesc. Health 2002, 31, 162–165, doi:10.1016/S1054-139X(02)00342-7.
[50]
Modan-Moses, D.; Yaroslavsky, A.; Novikov, I.; Segev, V.; Toledano, A.; Miterany, E.; Stein, D. Stunting of growth as a major feature of anorexia nervosa in male adolescents. Pediatrics 2003, 11, 270–276.
[51]
Swenne, I. Weight and growth requirements for menarche in teenage girls with eating disorders, weight loss and primary amenorrhea. Horm. Res. 2008, 69, 146–151, doi:10.1159/000112587.
[52]
Swenne, I.; Stridsberg, M.; Thurfjell, B.; Rosling, A. Insulin-like growth factor-1 as indicator of nutrition during treatment of adolescent girls with eating disorders. Acta Paediatr. 2007, 96, 1203–1208, doi:10.1111/j.1651-2227.2007.00400.x.
[53]
Swenne, I.; Borg, L.A.H.; Crace, C.J.; Schnell Landstr？m, A. Persistent reduction of pancreatic Beta-cell mass after a limited period of protein-energy malnutrition in the young rat. Diabetologia 1992, 35, 935–945.
[54]
Styrud, J.; Eriksson, U.J.; Grill, V.; Swenne, I. Experimental intrauterine growth retardation in the rat causes a reduction of pancreatic B-cell mass, which persists into adulthood. Biol. Neonate 2005, 88, 122–128, doi:10.1159/000086136.
[55]
Winick, M.; Noble, A. Cellular response in rats during malnutrition at various ages. J. Nutr. 1966, 89, 300–306.
[56]
Kliegman, R.M. Intrauterine Growth Retardation. In Neonatal-Perinatal Medicine: Diseases of the Fetus and Neonate, 6th; Fanaroff, A.A., Martin, R.J., Eds.; Mosby: St Louis, MO, USA, 1997; pp. 203–240.
[57]
Ngyuen, N.M.; Meyer, K.K.; Winick, M. Early malnutrition and “late” adoption: A study of their effects on the development of Korean orphans adopted into American families. Am. J. Clin. Nutr. 1977, 30, 1734–1739.
[58]
Black, R.E.; Allen, L.H.; Bhutta, Z.A.; Caulfield, L.E.; de Onis, M.; Ezzati, M.; Mathers, C.; Rivera, J. Maternal and Child Undernutrition Study Group. Maternal and child undernutrition: Global and regional exposures and health consequences. Lancet 2008, 371, 243–260.
[59]
Satyanaranyana, K.; Nadamuni Naidu, A.; Narasinga Rao, B.S. Adolescent growth spurt among rural Indian boys in relation to their nutritional status in early childhood. Ann. Hum. Biol. 1980, 7, 359–365, doi:10.1080/03014468000004431.
[60]
Martorell, R.; Rivera, J.; Kaplowitz, H. Consequences of stunting in early childhood for adult body size in rural Guatemala. Ann. Nestlé 1990, 48, 85–92.
[61]
Martorell, R.; Khan, L.K.; Schroeder, D.G. Reversibility of stunting: Epidemiological findings in children from developing countries. Eur. J. Clin. Nutr. 1994, 48, S45–S57.
[62]
Graham, G.G.; Adrianzen, B.; Rabold, J.; Mellits, E.D. Later growth of malnourished infants and children. Comparison with ‘healthy’ siblings and parents. Am. J. Dis. Child. 1982, 136, 348–352.
[63]
Proos, L.A.; Hofvander, Y.; Wennqvist, K.; Tuvemo, T. A longitudinal study on anthropometric and clinical development of Indian children adopted in Sweden. I. Clinical and anthropometric condition at arrival. Ups. J. Med. Sci. 1992, 97, 79–92, doi:10.3109/03009739209179285.
[64]
Proos, L.A.; Hofvander, Y.; Wennqvist, K.; Tuvemo, T. A longitudinal study on anthropometric and clinical development of Indian children adopted in Sweden. II. Growth, morbidity and development during two years after arrival in Sweden. Ups. J. Med. Sci. 1992, 97, 93–106, doi:10.3109/03009739209179286.
[65]
Kulin, H.E.; Bwibo, N.; Mutie, D.; Santner, S.J. The effect of chronic childhood malnutrition on pubertal growth and development. Am. J. Clin. Nutr. 1982, 36, 527–536.
[66]
Kulin, H.E.; Bwibo, N.; Mutir, D.; Santner, S.J. Gonadotropin excretion during puberty in malnourished children. J. Pediatr. 1984, 105, 325–328, doi:10.1016/S0022-3476(84)80141-9.
[67]
Gupta, N.; Singh, M.P.; Dhillon, B.S.; Saxena, N.C. Preparing for adulthood—Patterns of physical growth, sexual maturity and menarche of adolescent girls in selected urban slums and rural areas. J. Indian Med. Assoc. 2007, 105, 119–122.
[68]
Qamra, S.R.; Mehta, S.; Deodhar, S.D. A mixed-longitudinal study on the pattern of pubertal growth: Relationship to socioeconomic status and caloric intake—IV. Indian Pediatr. 1991, 28, 147–156.
[69]
Adair, L.S. Size at birth predicts age at menarche. Pediatrics 2001, 107, E59, doi:10.1542/peds.107.4.e59.
[70]
Adolfsson, S.; Westphal, O. Early pubertal development in girls adopted from Far-Eastern countries. Pediatr. Res. 1981, 15, 82. (abstract)., doi:10.1203/00006450-198101000-00068.
[71]
Proos, L.A.; Hofvander, Y.; Tuvemo, T. Menarcheal age and growth pattern in Indian Girls adopted in Sweden. II. Catch-up growth. Indian J. Pediatr. 1991, 58, 105–114, doi:10.1007/BF02810420.
[72]
Proos, L.A.; Hofvander, Y.; Tuvemo, T. Menarcheal age and growth pattern in Indian Girls adopted in Sweden. I. Menarcheal age. Acta Paediatr. Scand. 1991, 80, 852–858, doi:10.1111/j.1651-2227.1991.tb11960.x.
[73]
Proos, L.A.; Karlberg, J.; Hofvander, Y.; Tuvemo, T. Pubertal linear growth of Indian girls adopted in Sweden. Acta Paediatr. Scand. 1993, 82, 641–644.
[74]
Karlberg, J. A biologically-oriented mathematical model (ICP) for human growth. Acta Paediatr. Scand. 1989, Suppl. 350, 70–94, doi:10.1111/j.1651-2227.1989.tb11199.x.
[75]
Proos, L.A. Growth and development of Indian children adopted in Sweden. Indian J. Med. Res. 2009, 130, 646–650.
[76]
Oostdijk, W.; Yap, Y.N.; Rekers-Momberg, I.T.M.; Massa, G.G.; Brand, R.; Drop, S.L.S. The Impact of Early Puberty on Final Height in Foreign Born Adopted Children in the Netherlands. Central Precocious Puberty and Gonadotrophin Releasing Hormone Agonist Treatment. Ph.D. Dissertation 1996; Oostdijk, W., Ed.; Erasmus University, Rotterdam, The Netherlands, 1996; ISBN 90-9009946-8.
[77]
Virdis, R.; Street, M.E.; Zampolli, M.; Radetti, G.; Pezzini, B.; Benelli, M.; Ghizzoni, L.; Volta, C. Precocious puberty in girls adopted from developing countries. Arch. Dis. Child. 1998, 78, 152–154, doi:10.1136/adc.78.2.152.
[78]
Baron, S.; Battin, J.; David, A.; Limal, J.M. Precocious puberty in children adopted from foreign countries. Arch. Pediatr. 2000, 7, 809–816, doi:10.1016/S0929-693X(00)80189-X.
[79]
Kempers, M.J.E.; Otten, B.J. Idiopathic precocious puberty versus puberty in adopted children; auxological response to gonadotrophin—Releasing hormone agonist treatment and final height. Eur. J. Endocrinol. 2002, 147, 609–616, doi:10.1530/eje.0.1470609.
[80]
Mason, P.; Narad, C. Long-term growth and puberty concerns in international adoptees. Pediatr. Clin. North Am. 2005, 52, 1351–1368, doi:10.1016/j.pcl.2005.06.016.
[81]
Cataldo, F.; Accomando, S.; Porcari, V. Internationally adopted children: A new challenge for paediatricians. Minerva Pediatr. 2006, 58, 55–62.
[82]
Parent, A.-S.; Teilmann, G.; Juul, A.; Skakkebaek, N.E.; Toppari, J.; Bourguignon, J.-P. The timing of normal puberty and the age limits of sexual precocity: Variations around the world, secular trends, and changes after migration. Endocr. Rev. 2003, 24, 668–693, doi:10.1210/er.2002-0019.
[83]
Proos, L.A. Anthropometry in Adolescence—Secular trends, adoption, ethnic and environmental differences. Horm. Res. 1993, 39, 18–24, doi:10.1159/000182781.
[84]
Soriano-Guillén, L.; Corripio, R.; Labarta, J.I.; Canete, R.; Castro-Feijóo, L.; Espino, R.; Argente, J. Central precocious puberty in children living in Spain: Incidence, prevalence and influence of adoption and immigration. J. Clin. Endocrinol. Metabol. 2010, 9, 4305–4313.
[85]
Tuvemo, T.; Proos, L.A. Girls adopted from developing countries: A group at risk of early pubertal development and short final height. Implications for health surveillance and treatment. Ann. Med. 1993, 25, 217–219, doi:10.3109/07853899309147867.
[86]
Teilmann, G.; Pedersen, C.B.; Skakkebaek, N.E.; Jensen, T.K. Increased risk of precocious puberty in internationally adopted children in Denmark. Pediatrics 2006, 118, e391–e399, doi:10.1542/peds.2005-2939.
[87]
Teilmann, G.; Boas, M.; Petersen, J.H.; Main, K.M.; Gormsen, M.; Bamgaard, K.; Brocks, V.; Skakkebaek, N.E.; Jensen, T.K. Early pituitary-gonadal activation before clinical signs of puberty in 5- to 8-year-old adopted girls: A study of 99 foreign adopted girls and 93 controls. J. Clin. Endocrinol. Metab. 2007, 92, 2538–2544, doi:10.1210/jc.2006-2096.
[88]
Ebling, F.J.P. The neuroendocrine timing of puberty. Reproduction 2005, 126, 675–683, doi:10.1530/rep.1.00367.
[89]
Fernández-Fernández, R.; Navarro, V.M.; Barreiro, M.L.; Vigo, E.M.; Tovar, S.; Sirotkin, A.V.; Casanueva, F.F.; Aguilar, E.; Dieguez, C.; Pinilla, L.; Tena-Sempere, M. Effects of chronic hyperghrelinemia on puberty onset and pregnancy outcome in the rat. Endocrinology 2005, 146, 3018–3025.
[90]
Fernandez-Fernandez, R.; Martini, A.C.; Navarro, V.M.; Catellano, J.M.; Diguez, C.; Aguilar, E.; Pinilla, L.; Tena-Sempere, M. Novel signals for the integration of energy balance and reproduction. Mol. Cell. Endocrinol. 2006, 254-255, 127–132, doi:10.1016/j.mce.2006.04.026.
[91]
Barb, C.R.; Hausman, G.J.; Czaja, K. Leptin: A metabolic signal affecting central regulation of reproduction in the pig. Domest. Anim. Endocrinol. 2005, 29, 186–192, doi:10.1016/j.domaniend.2005.02.024.
[92]
Martos-Moreno, G.-á.; Chowen, J.A.; Argente, J. Metabolic signals in human puberty: Effects of over and undernutrition. Mol. Cell. Endocrinol. 2010, 324, 70–81.
[93]
Buck, G.M.; Gray, L.E., Jr.; Marcus, M.; Ojeda, S.R.; Pescovitz, O.H.; Witchel, S.F.; Sippell, W.; Abbott, D.H.; Soto, A.; Tyl, R.W.; et al. Environmental factors and puberty timing: Expert panel research needs. Pediatrics 2008, 121, S192–S207.
[94]
Toppari, J.; Juul, A. Trends in puberty timing in humans and environmental modifiers. Mol. Cell. Endocrinol. 2010, 324, 39–44, doi:10.1016/j.mce.2010.03.011.
[95]
Bourguignon, J.P.; Rasier, G.; Lebrethon, M.C.; Gérard, A.; Naveau, E.; Parent, A.S. Neuroendocrine disruption of pubertal timing and interactions between homeostasis of reproduction and energy balance. Mol. Cell. Endocrinol. 2010, 324, 110–120.
[96]
Krstevska-Konstantinova, M.; Charlier, C.; Craen, M.; Du Caju, M.; Heinrichs, C.; de Beaufort, C.; Plomteux, G.; Bourguignon, J.P. Sexual precocity after immigration from developing countries to Belgium: Evidence of previous exposure to organochlorine pesticides. Hum. Reprod. 2001, 16, 1020–1026.
[97]
Rasier, G.; Toppari, J.; Parent, A.-S.; Bourguignon, J.-P. Female sexual maturation and reproduction after prepubertal exposure to estrogens and endocrine disrupting chemicals: A review of rodent and human data. Mol. Cell. Endocrinol. 2006, 254-255, 187–201, doi:10.1016/j.mce.2006.04.002.
[98]
Skakkebaek, N.E.; Toppari, J.; S？der, O.; Gordon, C.M.; Divall, S.; Draznin, M. The exposure of fetuses and children to endocrine disrupting chemicals: A European Society for Paediatric Endocrinology (ESPE) and Pediatric Endocrine Society (PES) Call to action statement. J. Clin. Endocrinol. Metab. 2011, 26, 3056–3058.
[99]
Bourguignon, J.-P.; Gérard, A.; Alvarez Gonzalez, M.L.; Fawe, L.; Franchimont, P. Effects of changes in nutritional conditions on timing of puberty: Clinical evidence from adopted children and experimental studies in the male rat. Horm. Res. 1992, 38, S97–S105, doi:10.1159/000182579.
[100]
Foster, D.L.; Olster, D.H. Effects of restricted nutrition on puberty in the lamb: Patterns of tonic luteinizing hormone (LH) secretion and competency of the LH surge system. Endocrinology 1985, 116, 375–381.
[101]
Gopalan, C. Growth retardation in early childhood. Long term implications. NFI Bull. 2008, 29, 6–7.
[102]
Proos, L.A. Growth and development of Indian children adopted in Sweden. Indian J. Med. Res. 2009, 130, 646–650.
[103]
Lumey, L.H.; Stein, A.D. Offspring birth weights after maternal intrauterine undernutrition: A comparison within sibships. Am. J. Epidemiol. 1997, 146, 810–819, doi:10.1093/oxfordjournals.aje.a009198.
[104]
Schulz, L.C. The Dutch Hunger Winter and the developmental origins of health and disease. Proc. Natl. Acad. Sci. USA 2010, 107, 16757–16758, doi:10.1073/pnas.1012911107.
[105]
Heijmans, B.T.; Tobi, E.W.; Stein, A.D.; Putter, H.; Blauw, G.J.; Susser, E.S.; Slagboom, P.E.; Lumey, L.H. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. USA 2008, 105, 17046–17049.
[106]
Tobi, E.W.; Lumey, L.H.; Talens, R.P.; Kremer, D.; Putter, H.; Stein, A.D.; Slagboom, P.E.; Heijmans, B.T. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum. Mol. Genet. 2009, 18, 4046–4053, doi:10.1093/hmg/ddp353.
[107]
Greulich, W.W. A comparison of the physical growth and development of American-born and native Japanese children. Am. J. Phys. Anthropol. 1957, 15, 489–515, doi:10.1002/ajpa.1330150403.
[108]
Greulich, W.W. Some secular changes in the growth of American-born and native Japanese children. Am. J. Phys. Anthropol. 1976, 45, 553–568, doi:10.1002/ajpa.1330450320.
[109]
Ljung, B.O.; Bergsten-Brucefors, A.; Lindgren, G. The secular trend in physical growth in Sweden. Ann. Hum. Biol. 1974, 1, 245–256, doi:10.1080/03014467400000291.
[110]
Delmarre-van de Waal, H.A. Secular Trend of Timing of Puberty. In Abnormalities in Puberty. Scientific and Clinical Advances (Endocrine Development); Delemarre-van de Waal, H.A., Ed.; Karger: Basel, Switzerland, 2005; Volume 8, pp. 1–14.
[111]
Papadimitriou, A.; Nicolaidou, P.; Fretzayas, A.; Chrousos, G.P. Constitutional advancement of growth, a.k.a. early growth acceleration, predicts early puberty and childhood obesity. J. Clin. Endocrinol. Metab. 2010, 95, 4535–4541.
[112]
Papadimitriou, A.; Beri, D.; Tsialla, A.; Fretzayas, A.; Psychou, F.; Nicolaidou, P. Early growth acceleration in girls with idiopathic precocious puberty. J. Pediatr. 2006, 149, 43–46, doi:10.1016/j.jpeds.2006.02.005.
[113]
Tam, C.S.; de Zegher, F.; Garnett, S.P.; Baur, L.A.; Cowell, C.T. Opposing influences of prenatal and postnatal growth on the timing of menarche. J. Clin. Endocrinol. Metab. 2007, 92, 46–50.
[114]
Loucks, A.B. The response of luteinizing hormone pulsatility to 5 days of low energy availability disappears by 14 years of gynecological age. J. Clin. Endocrinol. Metab. 2006, 91, 3158–3164, doi:10.1210/jc.2006-0570.
