Prospective studies on growth in adopted Chinese girls are very scarce and are limited to short-term follow-ups of less than four years. The main purpose of these studies was to assess the degree of growth retardation upon arrival in the adoptive country and the degree of catch-up growth after adoption [1-6].

Growth retardation is a common finding in internationally adopted girls. Studies suggest that the cause may be related to phenomena such as malnutrition, stress and psychosocial deprivation prior to adoption [7-9].

The drastic change that occurs after adoption usually causes them to experience significant catch-up growth, but this can result in an acceleration of pubertal development. The pathophysiological mechanisms are not clear and possibly involve various endogenous and exogenous factors [9-12].

China has been the main country of origin for children adopted abroad by Spanish families [13]. China is a very large country in which genetic growth potential can vary between different geographic regions and socioeconomic classes [14].                

Aims and Objectives

The objectives of this study were to provide data on the longitudinal growth and timing of thelarche and menarche in adopted Chinese girls and comparison with the China growth and pubertal development references.

Observational epidemiological study of longitudinal design carried out on a cohort of 30 Chinese girls adopted by Spanish families between the years 2001-2007 in which growth and pubertal development were controlled after adoption during a 15-year follow-up in a specialized center of reference.

The total sample at the beginning of the study was 64 girls. Girls whose growth could not be controlled for 15 years (n = 33) and those who showed signs of pubertal development before 7 years of age and were referred to pediatric endocrinology for further evaluation of possible precocious puberty (n = 1) were excluded from the study.

The adopted Chinese girls studied had been abandoned for socioeconomic reasons and/or sexual discrimination within a few hours or days of their birth at the doors or near health centers, public buildings, or the orphanages themselves, thereby ensuring a quick reunion, reception and care. All were institutionalized until their adoption in orphanages in the southeast and southwest provinces of China (Jiangxi, Guangdong, Hunan, Fujian, Yunnan and Sichuan) (Figure 1).

Figure 1: Geographical Distribution of the 9 cities (their Corresponding Provinces are Shaded) in China where Girls were selected For the China Growth references. With a Red Dot, the Provinces of Origin of the Adopted Chinese Girls. Adapted from Zong XN and Li H [15]

The quality of the food and the health and psycho-affective care received during their institutionalization was questionable based on the information collected by the families in the orphanages and by the pre-adoption medical reports issued. Data on the health and nutritional status of the biological mother during pregnancy, gestational age and immediate neonatal period, anthropometric, health and educational family history and areas of residence (urban, suburban, or rural) were unknown.

Measurements

Weight, height and head circumference were measured and recorded in a standardized way, always by the same professional. The technical equipment used consisted of a Seca 708 electronic platform scale (Max 200 kg; d = 0.1 kg) with a built-in stadiometer for height, GC-1104 children's electronic scale (Max 20 kg; d = 10 g), horizontal board for length (Max 100 cm) for children under 3 years and a flexible non-stretchable plastic tape measure. The anthropometric parameter values were entered into an Excel sheet with which the arithmetic mean, Standard Deviation (SD) and Body Mass Index (BMI = kg/m²) were calculated. Families were instructed to detect thelarche and menarche and to carry out control after their appearance. The age values were entered into an Excel sheet with which the arithmetic mean, the SD and the median were calculated. The anthropometric parameters values and ages at thelarche and menarche, were compared with the China growth and pubertal development references.

The procedures used in the patients were performed after obtaining informed consent from the legal guardian. The data was used in accordance with Organic Law 3/2018 on the Protection of Personal Data and Guarantee of Digital Rights in force in Spain.

Statistical Analysis

Through the Social Science Statistics ©2023 operating system, the mean values obtained from the anthropometric parameters were compared with the China growth references for girls [15], calculating the Z-score and the p-value with a significance level <0.05. Significant catch-up growth was defined when the Z-score of the parameter had an increase > +0.5 SD. The graphs were prepared with the Excel calculation program.

Table 1 shows the values of weight, height, BMI and head circumference of the adopted Chinese girls obtained at the initial evaluation after the adoption and in the annual controls during a 15-year follow-up.

Table 1: Values of Weight, Height, Body Mass Index and Head Circumference of Adopted Chinese Girls (N = 30) at Initial Evaluation after Adoption and During A 15-Year Follow-Up

*Initial evaluation after adoption; BMI: Body Mass Index, SD: Standard Deviation

The mean age at which the initial evaluation was carried out was 1.33 years. The mean age of onset of thelarche (Tanner stage 2) was 10.08 years (median, 10 years). The mean age at menarche presentation was 12.17 years (median, 12.5 years).

Figures 2-5 compare the curves of mean values for the age of weight, height, BMI and head circumference of Chinese girls adopted with the China growth references for girls.

Weight-for-age (Figure 2). 

Figure 2: Weight-for-Age of Adopted Chinese Girls Compared with the China Growth References for Girls

At initial evaluation, Z-score was -1.55. At 2 years of age, there had been significant catch-up growth (Z-score -0.74). In longitudinal evolution, adopted Chinese girls weighed less up to 14 years, mainly between 10-12 years and weighed more between 15-16 years. At 16 years the weight was +0.64 kg. No statistically significant differences were found.

Height-for-age (Figure 3).

Figure 3: Height-for-Age of Adopted Chinese Girls Compared with the China Growth References for Girls

 At initial evaluation, Z-score was -1.4. At 2 years of age, there had been significant catch-up growth (Z-score -0.62). In longitudinal evolution, adopted Chinese girls were smaller at all ages, mainly between 10-12 years. At 16 years of age, the height was -2.83 cm. No statistically significant differences were found.

BMI-for-age (Figure 4). 

Figure 4: BMI-for-Age of adopted Chinese Girls Compared with the China Growth References for Girls

At initial evaluation, Z-score was -0.72. At 2 years of age, Z-score was -0.38. In longitudinal evolution, it was lower in adopted Chinese girls between 1.33-2 years and 10-12 years and higher between 14-16 years. At 16 years of age, the BMI was +1.08 kg/m². No statistically significant differences were found.

Head circumference-for-age (Figure 5). 

Figure 5: Head Circumference-for-Age of Adopted Chinese girls Compared with the China Growth References for Girls

At initial evaluation, the Z-score was -1.1. At 6 years of age, there had been no significant catch-up growth (Z-score -0.74). In longitudinal evolution, it was lower in adopted Chinese girls at all ages, mainly between 1.33-2 years. 

At 6 years of age, the head circumference was -0.96 cm. No statistically significant differences were found.

To our knowledge, this is the first prospective study on long-term growth in adopted Chinese girls with a 15-year follow-up.

The China growth references for girls were developed in 2005 with a sample of 47,213 girls randomly selected from the urban areas of 9 major cities (Beijing, Shanghai, Harbin, Xi'an, Nanjing, Wuhan, Guangzhou, Fuzhou and Kunming) (Figure 1). The reference sample was representative of a healthy and relatively well-nourished population that was born and raised in good conditions, with high living standards and educational level (80.6-84.4% of mothers and fathers, respectively, of these girls had secondary education or higher; the overall breast-feeding rate was 85.1% and exclusive breastfeeding 47.7%). Exclusion criteria included temporary residents, history of premature birth, birth weight less than 2,500 g, chronic illness, obviously malnourished, physically handicapped and acute illness within the screening period [15].

The characteristics of the studied cohort of adopted Chinese girls were previously described and it is clear that we are comparing a cohort of disadvantaged girls from an early age until their adoption with a national sample of girls privileged from birth.

All short-term prospective studies on growth in adopted Chinese girls observed delayed weight, height and head circumference at initial post-adoption assessment, with Z-scores between -1 and -2 SD with respect to the reference standards used (World Health Organization or national standards of the adoptive country) [1-6].

Studies with follow-up between 1 and 3 years after adoption have shown significant weight recovery between 6-12 months and height between 12-24 months [4-6] Van Ijzendoorn et al. [16], through a meta-analysis study, calculated the differences in rates of stunting between internationally adopted children and reference populations. In adopted children, they observed that at the time of adoption, they presented significant delays in weight, height and head circumference and that after adoption they showed almost complete recovery of weight and height, but recovery of head circumference was slower and remained incomplete. They concluded that international adoption leads to a substantial recovery of weight and height, but not head circumference, demonstrating the differential plasticity of children's physical growth.

These short-term growth findings were corroborated in our study's cohort of adopted Chinese girls and with respect to observed delays, no significant differences were found compared with the China growth references.

Regarding the longitudinal growth pattern of the cohort of adopted Chinese girls, although no significant differences were found with the China growth references, the main divergences were as follows. The nutrition level of the adopted Chinese girls was lower than that of the China girls up to the age of 14, from which age the nutrition level was higher. The height level of adopted Chinese girls was lower than that of the China girls at all ages. According to the China growth references for girls, height after age 15 is very close to adult height [15]. The head circumference of the adopted Chinese girls was smaller than that of the China girls at all ages.

Concerning pubertal development, Ma et al. [17], in a cross-sectional study on a nationally representative sample of 20,654 Chinese girls, determined the median age of thelarche and menarche at 9.20 years and 12.27 years, respectively. Sun et al. [18], in a cross-sectional study on a nationally representative sample of 15,388 Chinese girls of the Han ethnic group, determined the median age of thelarche and menarche at 9.18 years and 12.43 years, respectively and that urban girls reached menarche at a much earlier age than rural girls. Liang et al. [19], in a recent cross-sectional study on a nationally representative sample of 108,343 Chinese girls, determined the median age at thelarche and menarche to be 9.65 years and 12.39 years, respectively. Hayes et al. 20] in a survey study of parents of 814 Chinese girls adopted in North America, estimated the median age at menarche to be 12.37 years and the pre-10-year prevalence to be 3%. Tan et al. [21] studied 298 Chinese girls with an age range of 7.3-11.1 years, adopted in North America at 1.05 years and observed that in 3.5% thelarche appeared before the 8 years and 2.3% presented menarche before the age of 11.

In the studied cohort of adopted Chinese girls, compared to the national studies from China, the age of onset of thelarche was slightly later and the age of menarche was similar. In 3.3%, the thelarche appeared before the age of 8 and 6.6% presented menarche before the age of 11. A phenomenon that we do not know how to interpret is the fact that between thelarche and menarche was the period in which the greatest difference was observed, by default, in weight and height with respect to the China growth references (Figures 2 and 3).

It is known that growth and pubertal development are determined by endogenous factors (genetic, epigenetic, metabolic and neurohormonal) that interact throughout the entire process with a multitude of exogenous factors (food, nutrition, hygiene, medical care, chronic diseases, climate affective, psychosocial environment, stress, environmental variables, etc.). So that the genetic potential is not altered, it is essential that all the factors work correctly and are balanced [7,8,22-25] 

Although we cannot justify it pathophysiologically, we believe that various exogenous factors may be involved in the pattern of growth and pubertal development that we have observed in the cohort of adopted Chinese girls.

In the cohort of adopted Chinese girls, the growth potential was lower and the pubertal development was slightly later, although without significant differences, compared with the China growth and pubertal development references.

1. Miller, L.C. and N.W. Hendrie. “Health of children adopted from China.” Pediatrics, vol. 105, no. 6, 2000, article E76, https://doi.org/10.1542/peds.105.6.e76.

2. Pomerleau, A. et al. “Health status, cognitive and motor development of young children adopted from China, East Asia and Russia across the first six months after adoption.” Journal of Applied Developmental Psychology, vol. 29, no. 5, 2005, pp. 445–457, https://doi.org/10.1177/016502505 0020625.

3. Oliván Gonzalvo, G. “Estudio Auxológico de Niñas Adoptadas en China [Auxologic Study of Girls Adopted in China].” Anales de Pediatría, vol. 65, no. 1, 2006, pp. 88–90, https://doi.org/10.1157/13090906.

4. Cohen, N.J. et al.“Children Adopted from China: A Prospective Study of Their Growth and Development.” Journal of Child Psychology and Psychiatry, vol. 49, no. 4, 2008, pp. 458–468, https://doi.org/10.1111/j.1469-7610.2007.01853.x.

5. Palacios, J. et al. “Growth and development in internationally adopted children: Extent and timing of recovery after early adversity.” Child: Care, Health and Development, vol. 37, no. 2, 2011, pp. 282–288, https://doi.org/10.1111/j.1365-2214.2010.01142.x.

6. Canzi, E. et al. “Growth recovery in newly arrived international adoptees in Italy: Relation to parenting stress.” Minerva Pediatrica, vol. 73, no. 4, 2021, pp. 316–323, https://doi.org/10.23736/S2724-5276.18.05155-1.

7. Gat-Yablonski, G. and F. DeLuca. “Effect of nutrition on statural growth.” Hormone Research in Paediatrics, vol. 88, no. 1, 2017, pp. 46–62, https://doi.org/10.1159/000456547.

8. Mousikou, M. et al. “Stress and growth in children and adolescents.” Hormone Research in Paediatrics, vol. 96, no. 1, 2023, pp. 25–33, https://doi.org/10.1159/000521074.

9. Mason, P. and C. Narad. “Long-term growth and puberty concerns in international adoptees.” Pediatric Clinics of North America, vol. 52, no. 5, 2005, pp. 1351–1368, https://doi.org/10.1016/j.pcl.2005.06.016.

10. Dominé, F. et al. “Assessment and mechanism of variations in pubertal timing in internationally adopted children: a developmental hypothesis.” European Journal of Endocrinology, vol. 155, suppl. 1, 2006, pp. S17–S25, https://doi.org/10.1530/eje.1.02252.

11. Teilmann, G. et al. “Early puberty in internationally adopted girls: hormonal and clinical markers of puberty in 276 girls examined biannually over two years.” Hormone Research, vol. 72, no. 4, 2009, pp. 236–246, https://doi.org/10.1159/000236085.

12. Stagi, S. et al. “Auxological and endocrinological features in internationally adopted children.” Italian Journal of Pediatrics, vol. 46, 2020, article 82, https://doi.org/10.1186/s13052-020-00832-5.

13. Oliván Gonzalvo, G. “Estado de Salud de Niños Adoptados en China [Health Status of Children Adopted from China].” Revista Pediatría de Atención Primaria, vol. 8, no. 32, 2006, pp. 605–613.

14. Li, H. et al. “Physical growth of children in urban, suburban and rural mainland China: A Study of 20 Years Change.” Biomedical and Environmental Sciences, vol. 24, no. 1, 2011, pp. 1–11, https://doi.org/10.3967/0895-3988. 2011.01.001.

15. Zong, X.N. and H. Li. “Construction of a new growth references for China based on urban Chinese children: comparison with the WHO growth standards.” PLoS One, vol. 8, no. 3, 2013, article e59569, https://doi.org/10.1371/journal.pone.0059569.

16. Van Ijzendoorn, M.H. et al. “Plasticity of growth in height, weight and head circumference: Meta-analytic evidence of massive catch-up after international adoption.” Journal of Developmental and Behavioral Pediatrics, vol. 28, no. 4, 2007, pp. 334–343, https://doi.org/10.1097/DBP .0b013e31811320aa.

17. Ma, H.M. et al. “Onset of breast and pubic hair development and menses in urban Chinese Girls.” Pediatrics, vol. 124, no. 2, 2009, pp. e269–e277, https://doi.org/10.1542/peds. 2008-2638.

18. Sun, Y. et al. “National estimates of the pubertal milestones among urban and rural Chinese girls.” Journal of Adolescent Health, vol. 51, no. 3, 2012, pp. 279–284, https://doi.org/10.1016/j.jadohealth.2011.12.019.

19. Liang, X. et al. “Current pubertal development in Chinese children and the impact of overnutrition, lifestyle and perinatal factors.” Journal of Clinical Endocrinology and Metabolism, 2023, article dgad102, https://doi.org/ 10.1210/clinem/dgad102.

20. Hayes, P. and T.X. Tan. “Timing of menarche in girls adopted from China: A cohort study.” Child: Care, Health and Development, vol. 42, no. 6, 2016, pp. 859–862, https://doi.org/10.1111/cch.12393.

21. Tan, T.X. and L.A. Camras. “Pre-menarche pubertal development following unique form of immigration: The case of girls adopted from China.” Journal of Immigrant and Minority Health, vol. 17, no. 1, 2015, pp. 232–238, https://doi.org/10.1007/s10903-013-9908-3.

22. Nilsson, O. “Growth and growth disorders in 2017: Genetic and epigenetic regulation of childhood growth.” Nature Reviews Endocrinology, vol. 14, no. 2, 2018, pp. 70–72, https://doi.org/10.1038/nrendo.2017.178.

23. Benyi, E. and L. Sävendahl. “the physiology of childhood growth: Hormonal regulation.” Hormone Research in Paediatrics, vol. 88, no. 1, 2017, pp. 6–14, https://doi.org/10.1159/000471876.

24. Hermanussen, M. et al. “The socio-endocrine regulation of human growth.” Acta Paediatrica, vol. 111, no. 11, 2022, pp. 2077–2081, https://doi.org/10.1111/apa.16504.

25. McEwen, B.S. “Understanding the potency of stressful early life experiences on brain and body function.” Metabolism, vol. 57, suppl. 2, 2008, pp. S11–S15, https://doi.org/10.1016/j.metabol.2008.07.006.