INTRODUCTION

Growth is 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, emotional climate, psychosocial environment, stress, environmental variables, etc.). In such a way that so that the genetic potential of growth is not altered, all factors must function correctly and balanced [1, 2, 3, 4].

They have internationally adopted children frequently present factors that can affect growth, highlighting, among others, adverse prenatal exposures (drugs, alcohol, etc.), intrauterine growth retardation, prematurity, perinatal hypoxia, psycho-affective deprivation, abuse and neglect, stress, malnutrition, and micronutrient deficiencies. Furthermore, growth deficiency may be permanent, even if other factors (nutrition, health, psychosocial environment, etc.) improve later [5, 6, 7, 8].

Russia has been one of the main countries of origin for children adopted abroad by Spanish families [9]. Prospective studies on the growth of children adopted from Russia are scarce. They are limited to short-term follow-ups, between 3 weeks and 1 year, evaluating the degree of delay upon arrival in the adoptive country and recovery after adoption [10, 11, 12, 13]. To our knowledge, only one study has conducted a 3-year follow-up after adoption [14], with no longer-term prospective studies published. The objective of this study is to contribute data on the temporal trends in weight, height, body mass index (BMI), and head circumference in boys adopted from Russia.

MATERIAL AND METHODS

An observational epidemiological study with a longitudinal design was carried out on an initial cohort of 139 Russian boys adopted in Spain between 2001 and 2013, in which growth was monitored in a specialized reference center. All the children resided in orphanages until their adoption. Upon arrival, pre-adoption medical records were reviewed to collect data on gestational age, birth weight, prenatal alcohol exposure, and reasons for institutionalization. During follow-up, for different reasons, subjects were lost, and two who were diagnosed with fetal alcohol syndrome and one with growth hormone deficiency were excluded. In those adopted after 2006, the follow-up was less than fourteen years.

Weight, height, and head circumference were measured and recorded in a standardized manner in the initial post-arrival evaluation and in the annual follow-up checks, always performed by the same clinician. 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 electronic children's scale (Max 20 kg; d = 10 g), lengthboard Seca (Max 100 cm) for children under 3 years and inextensible millimeter measuring tape. We entered data for the study variables in an Excel spreadsheet, also used to calculate the mean, standard deviation (SD), and body mass index (BMI = kg/m2). The procedures used in the patients were carried out after obtaining the informed consent of the legal guardian. The data were used under Organic Law 3/2018 on the Protection of Personal Data and Guarantee of Digital Rights in force in Spain.

Using the WHO Anthro v3.2.2 (0-5 years) and WHO AnthroPlus v1.0.4 (5-19 years) operating systems [15], we compared the anthropometric measurements obtained in the sample with the World Health Organization (WHO) child growth standards [16]. The corresponding z-scores were calculated, which indicates how many SDs above or below the mean a value is located, and percentiles for age and sex (note: these applications do not calculate the z-score or percentile of the head circumference from age 5 years or of the weight from age 10 years). A z-score value for any given variable of +/-0.5 SDs or greater to WHO standards was considered as a reference point for anthropometric relevant differences. According to the WHO child growth standards, a z-score of the variable < -2 SD defines severe retardation, and between -1 and -2 SD defines moderate retardation. We defined significant catch-up growth for any given variable as a z-score annual increase of +0.5 SDs or greater.

RESULTS

The main history of the adopted Russian boys´ cohort was born preterm (32.4%), low birth weight (26.6%), documented prenatal alcohol exposure (19.4%), abandonment at birth (56, 1%), and abuse/neglect (49.3%).

Table 1 presents the anthropometric measurements obtained in the initial post-arrival evaluation (mean age, 3 years) and during the annual follow-up controls, comparing them with the WHO child growth standards. Figure 1 shows the temporal trends in the height and BMI z-scores using the WHO child growth standards as reference. The main findings are described below.

Weight: in the initial post-arrival evaluation they showed moderate delay (15.1% < -2 SD); in the first year post-adoption, significant catch-up growth was observed (z-score increase, +0.73); at age 4 years, relevant delay persisted; from age 5 years, in the longitudinal analysis, no anthropometric relevant differences were observed to WHO standards. Height: in the initial post-arrival evaluation, they showed severe delay (47.5% < -2 SD). In the first and second year post-adoption, significant catch-up growth was observed (z-score increase, +1.05 and +0.58, respectively); at age 6 years, relevant delay persisted; in the longitudinal analysis, from ages 7 to 11 years a gradual increase was observed, and from ages 12 to 17 years a gradual decrease, no showing anthropometric relevant differences to WHO standards. BMI: the longitudinal analysis showed that the degree of height delay was always greater than that of weight, balancing after age 14 years. Head circumference: in the initial post-arrival evaluation they showed moderate delay (7.2% < -2 SD); in the first year post-adoption, significant catch-up growth was observed (z-score increase, +0.6); at age 5 years, no anthropometric relevant difference was observed to WHO standards.

DISCUSSION

Measurements of weight, height, and head circumference are a simple method of assessing growth, providing a useful index of child health and development [16]. Furthermore, the measurement of head circumference is directly related to brain size, with its development during early childhood being a key determinant of later cognition, learning, and behavior [17].

Russia is a very large country in which genetic growth potential can vary between different geographic regions and socioeconomic environments. Martinchik et al. [18] compared the mean values of weight, height, and BMI of the Russian child population with the WHO child growth standards. Analysis of z-score values of the anthropometric parameters showed that the most relevant difference was the high positive mean values of BMI z-score in the age of 0-6 years. They concluded that the use of WHO standards could be recommended for assessing the growth and nutrition of children in Russia.

Growth delay at the time of adoption is a common finding in children adopted from Russia. Observational studies indicate that the cause is probably related to late adoption and adverse pre-adoption factors, primarily prenatal alcohol exposure, prematurity, low birth weight, psycho-affective deprivation, stress, and malnutrition. [9, 10, 11, 12, 13, 14]. The drastic change that occurs after adoption means that they generally experience significant catch-up growth [10, 11, 13, 14] but this can lead to an acceleration of pubertal development [8, 19] and an increased risk of developing puberty precocious [20]. The pathophysiological mechanisms are unclear and possibly involve various endogenous and exogenous factors [21].

In adopted Russian children, regression analysis studies [10, 12, 13] and a meta-analysis study [22], have determined that prenatal alcohol exposure, low birth weight, a higher degree of malnutrition at the time of adoption, and late adoption, are independent predictors of greater delay in height and head circumference in the initial evaluation after adoption. In addition, that early adoption, a greater degree of initial growth retardation, and greater caloric intake after adoption are associated with better and more complete catch-up growth.

In the studied cohort of adopted Russian boys, the prevalence of prematurity, low birth weight, and initial malnutrition was 8, 5, and 7 times higher, respectively, than in the general Russian child population [23]. The prevalence of documented prenatal alcohol exposure was 2 times lower than that observed in institutionalized Russian children [24]. The prevalence of fetal alcohol syndrome was 7 and 5 times lower, respectively, than that observed in institutionalized [25] or adopted Russian children [12]. Finally, the mean age at adoption was 2 times later than that observed in other studies of Russian adopted children [12, 13, 14].

Regarding the growth pattern of the adopted Russian boys’ cohort, in the initial evaluation after adoption, moderate delay in weight and head circumference, and severe delay in height, were observed. Compared with observations by other researchers [12, 14], the mean value of the weight z-score was similar, the mean value of the height z-score was 2 times lower, and the mean value of the head circumference z-score was intermediate. According to other researchers [10, 11, 12, 13, 14, 22], it is likely that the interaction of adverse factors (prematurity, prenatal alcohol exposure, low birth weight, abuse and neglect, initial malnutrition, and late adoption), observed with frequency in this cohort of adopted Russian boys, explain the severe delay in height and moderate delay in head circumference at the time of adoption.

In the first year after adoption, significant recovery growth in weight, height, and head circumference was observed. In the second year, recovery growth was observed in all anthropometric parameters, although it was only significant for height. In the third year after adoption, they no longer presented relevant delays in weight and head circumference, and in the fourth, neither in height. These findings were similar to those observed by other researchers [10, 11, 13, 14, 22], although the recovery of height was later probably due to its greater delay at the time of adoption.

During the longitudinal analysis, the BMI z-score showed that the degree of delay in height was always greater than that of weight, balancing after age 14 years; the height z-score showed a gradual increase from age 7 to 11 years, and a gradual decrease from age 12 to 17 years, no showing relevant differences to WHO standards. During the study period, despite the rapid, intense, and prolonged catch-up growth, no child developed precocious puberty.

CONCLUSIONS

In the cohort of boys adopted from Russia, these findings suggest that, despite the important delay in height, weight, and head circumference at the time of adoption, and the various factors adverse to growth, international adoption led to a substantial recovery of all anthropometric parameters, manifesting plasticity in the physical growth of these children.

CONFLICT OF INTERESTS

The authors have no conflict of interest to declare. The authors declared that this study has received no financial support.

REFERENCES

1.Nilsson O. Growth and growth disorders in 2017: Genetic and epigenetic regulation of childhood growth. Nat Rev Endocrinol. 2018;14(2):70-2. doi: 10.1038/nrendo.2017.178.

2.Benyi E, Sävendahl L. The Physiology of Childhood Growth: Hormonal Regulation. Horm Res Paediatr. 2017;88(1):6-14. doi: 10.1159/000471876.

3.Gat-Yablonski G, De Luca F. Effect of Nutrition on Statural Growth
. Horm Res Paediatr. 2017;88(1):46-62. doi: 10.1159/000456547.

4.Mousikou M, Kyriakou A, Skordis N. Stress and Growth in Children and Adolescents. Horm Res Paediatr. 2023;96(1):25-33. doi: 10.1159/000521074.

5.Park H, Bothe D, Holsinger E, Kirchner HL, Olness K, Mandalakas A. The impact of nutritional status and longitudinal recovery of motor and cognitive milestones in internationally adopted children. Int J Environ Res Public Health. 2011;8(1):105-16. doi: 10.3390/ijerph8010105.

6.Miller BS, Spratt EG, Himes JH, Condon D, Summer A, Papa CE, et al. Growth failure associated with early neglect: pilot comparison of neglected US children and international adoptees. J Pediatr Endocrinol Metab. 2015;28(1-2):111-5. doi: 10.1515/jpem-2014-0231.

7.Schoenmaker C, Juffer F, van IJzendoorn MH, van den Dries L, Linting M, van der Voort A, et al. Cognitive and health-related outcomes after exposure to early malnutrition: the Leiden longitudinal study of international adoptees. Child Youth Serv Rev. 2015;48:80-6. doi: 10.1016/j.childyouth.2014.12.010.

8.Mason P, Narad C. Long-term growth and puberty concerns in international adoptees. Pediatr Clin North Am. 2005;52(5):1351-68, vii. doi: 10.1016/j.pcl.2005.06.016.

9.Oliván Gonzalvo G. [Adoption in the Russian Federation and Eastern Europe: health problems and medical recommendations]. Rev Pediatr Aten Primaria. 2006;8(30):265-81.

10.Judge S. Developmental recovery and deficit in children adopted from Eastern European orphanages. Child Psychiatry Hum Dev. 2003;34(1):49-62. doi: 10.1023/a:1025302025694.

11.Pomerleau A, Malcuit G, Chicoine JF, Seguin R, Belhumeur C, Germain P, 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. J Appl Dev Psychol. 2005;29(5):445-57. doi: 10.1177/0165025050020625.

12.Miller BS, Kroupina MG, Iverson SL, Masons P, Narad C, Himes JH, et al. Auxological evaluation and determinants of growth failure at the time of adoption in Eastern European adoptees. J Pediatr Endocrinol Metab. 2009;22(1):31-9. doi: 10.1515/jpem.2009.22.1.31.

13.Miller BS, Kroupina MG, Mason P, Iverson SL, Narad C, Himes JH, Johnson DE, Petryk A, et al. Determinants of catch-up growth in international adoptees from eastern europe. Int J Pediatr Endocrinol. 2010;2010:107252. doi: 10.1155/2010/107252.

14.Palacios J, Román M, Camacho C. Growth and development in internationally adopted children: extent and timing of recovery after early adversity. Child Care Health Dev. 2011;37(2):282-8. doi: 10.1111/j.1365-2214.2010.01142.x.

15.World Health Organization. Child Growth Standards. The WHO Anthro Software. 2023. Available from: https://www.who.int/tools/child-growth-standards/software (accessed Nov 2023).

16.World Health Organization. Child Growth Standards. 2023. Available from: https://www.who.int/tools/child-growth-standards (accessed Nov 2023).

17.Bartholomeusz HH, Courchesne E, Karns CM. Relationship between head circumference and brain volume in healthy normal toddlers, children, and adults. Neuropediatrics. 2002;33(5):239-41. doi: 10.1055/s-2002-36735.

18.Martinchik AN, Baturin AK, Keshabyants EE, Peskova EV. [Retrospective assessment of anthropometric measurements of children in Russia 1994–2012 according to the new WHO standards]. Pediatria n.a. G.N. Speransky. 2015;94(1):156-60. doi: 10.15690/pf.v13i4.1608.

19.Dominé F, Parent AS, Rasier G, Lebrethon MC, Bourguignon JP. Assessment and mechanism of variations in pubertal timing in internationally adopted children: a developmental hypothesis. Eur J Endocrinol. 2006;155(1):S17-S25. doi: 10.1530/eje.1.02252.

20.Teilmann G, Pedersen CB, Skakkebaek NE, Jensen TK. Increased risk of precocious puberty in internationally adopted children in Denmark. Pediatrics. 2006;118(2):e391-9. doi: 10.1542/peds.2005-2939.

21.Stagi S, Papacciuoli V, Boiro D, Maggioli C, Ndambao NN, Losi S, et al. Auxological and endocrinological features in internationally adopted children. Ital J Pediatr. 2020;46(1):82. doi: 10.1186/s13052-020-00832-5.

22.Van Ijzendoorn MH, Bakermans-Kranenburg MJ, Juffer F. Plasticity of growth in height, weight, and head circumference: meta-analytic evidence of massive catch-up after international adoption. J Dev Behav Pediatr. 2007;28(4):334-43. doi: 10.1097/DBP.0b013e31811320aa.

23.Oliván-Gonzalvo G. [Prevalence of prematurity, low birth weight and malnutrition in early childhood in Russian children assigned for international adoption]. An Pediatr (Engl Ed). 2019;91(3):214-5. doi: 10.1016/j.anpedi.2019.04.011.

24.Miller LC, Chan W, Litvinova A, Rubin A, Tirella L, Cermak S. Medical diagnoses and growth of children residing in Russian orphanages. Acta Paediatr. 2007;96(12):1765-9. doi: 10.1111/j.1651-2227.2007.00537.x.

25.Olivan-Gonzalvo G. [Frequency of fetal alcohol syndrome in institutionalized children of eastern European countries]. Rev Neurol. 2011;53(2):127-8.

Notas de autor

golivang@gmail.com

IR