Skip to main content

ORIGINAL RESEARCH article

Front. Endocrinol., 08 September 2021
Sec. Pediatric Endocrinology

Estimation of Pubertal Growth Spurt Parameters in Children and Adolescents Living at Moderate Altitude in Colombia

Marco Antonio Cossio-BolaosMarco Antonio Cossio-Bolaños1Ruben Vidal-EspinozaRuben Vidal-Espinoza2Juan Minango-NegreteJuan Minango-Negrete3Pedro R. Olivares,Pedro R. Olivares4,5Luis Urzua-AlulLuis Urzua-Alul6Luis Felipe Castelli Correia de CamposLuis Felipe Castelli Correia de Campos7Jose Fuentes-LpezJose Fuentes-López8Lucila Sanchez-MacedoLucila Sanchez-Macedo8Edilberto Diaz-BonillaEdilberto Diaz-Bonilla9Claudia Torres-GalvisClaudia Torres-Galvis9Rossana Gomez-Campos*Rossana Gomez-Campos10*
  • 1Department of Physical Activity Sciences, Faculty of Education Sciences, Catholic University of the Maule, Talca, Chile
  • 2Universidad Católica Silva Henríquez, Santiago, Chile
  • 3Instituto Superior Universitario Rumiñahui, Sangolqui, Quito, Ecuador
  • 4Faculty of Education, Psychology and Sport Sciences University of Huelva, Huelva, Spain
  • 5EFISAL Research Group, Universidad Autonoma de Chile, Talca, Chile
  • 6Escuela de Kinesiología, Facultad de Salud, Universidad Santo Tomás, Santiago, Chile
  • 7Department of Education Sciences, Faculty of Education and Humanities, University of Bío Bío, Chillan, Chile
  • 8Instituto de Investigación en Ciencias de la Educación (IICE), Universidad Nacional del Altiplano de Puno, Puno, Perú
  • 9Universidad Pedagógica y Tecnológica de Colombia, Tunja, Colombia
  • 10Department of Educational Diversity and Inclusivity, Catholic University of the Maule, Talca, Chile

Objective: Knowledge of the biological parameters of pubertal growth spurt allows verification of secular changes and exploration of the timing of puberty. The aim of the study was to estimate final height, age at peak height velocity (APHV), and peak height velocity PHV (cm/y) in children and adolescents living at moderate altitude in Colombia.

Methods: A cross-sectional study was designed in 2.295 schoolchildren from Bogotá (Colombia) with an age range from 5.0 to 18.9 years. Height (cm) was assessed. Preece–Baines model 1 (1PB) was used to make inferences about mathematical and biological parameters.

Results: The five mathematical parameters estimated in general have reflected quality in the fit to the model, reflecting a small residual error. Final height was reached in boys at 170.8 ± 0.4 cm and in girls at 157.9 ± 0.2 cm. APHV was estimated at 12.71 ± 0.1 years in boys and 10.4 ± 0.2 years in girls. Girls reached APHV 2.2 years earlier than boys. In relation to PHV (cm/y), boys reached higher growth speed in height (7.4 ± 0.4 cm/y), and in girls it was (7.0 ± 0.2 cm/y).

Conclusion: It was determined that final height was reached at 170.8 ± 0.4 cm in boys and 157.9 ± 0.2 cm in girls, and APHV (years) and PHV (cm/ye) were reached relatively early and with average peak velocity similar to Asian and Western populations. A large-scale longitudinal study is needed to confirm these findings.

Introduction

Human growth is traditionally conceived as a goal-seeking process regulated by genes, nutrition, health, and the state of an individual’s social and economic environment (1, 2). It is characterized by extraordinary plasticity and population heterogeneity (3).

It is considered fundamental for planning the promotion of health programs and serves as a basis for pediatricians to assess diseases with possible growth disturbances (4). Its assessment can be made from longitudinal, cross-sectional, mixed longitudinal, or linked longitudinal studies (1). However, to determine growth velocity, a longitudinal study should be used before a cross-sectional study (5).

In fact, conducting a longitudinal study involves long periods of time, often years or decades (6), which makes the process of collecting data continuously difficult although, in general, in recent years, the estimation of peak growth velocity and pubertal growth spurt parameters in children and adolescents from various parts of the world (4, 7, 8) have been determined by mathematical models, specifically Preece–Baines (9) model 1 (1PB).

Consequently, based on the fact that children and adolescents have varied growth rates (1) in general, girls average a maximum height velocity of 9 cm/y at age 12 years, and boys, on average, reach a maximum height velocity of 10.3 cm/y at age 14 years (1, 10, 11) this study assumes that children and adolescents living at moderate altitude in Bogotá, Colombia, could reflect similar growth patterns to those reported by the literature.

Therefore, the objective of the study was to estimate final height, age at peak height velocity (APHV), and peak height velocity (PHV) (cm/y) in children and adolescents living at moderate altitude in Colombia. These parameters are determined by means of 1PB (9) as an alternative means of approximating longitudinal growth patterns.

Materials and Methods

Type of Study and Sample

A descriptive (cross-sectional) study was carried out in 2295 schoolchildren (1175 boys and 1120 girls) in Bogotá (Colombia). This city is the capital of Colombia and is located 2640 m above sea level. The sample selection was nonprobabilistic (quotas). The age range was 5 to 18.9 years.

The schoolchildren participated voluntarily in the study. Parents signed a consent form, and children and adolescents signed an informed consent form. Schoolchildren who were within the school age range (primary and secondary level) and those who completed the anthropometric evaluations were included. Those with any type of physical injury and children who were foreigners were excluded. The study was conducted in accordance with Resolution 8430 of the Colombian Ministry of Health and Social Protection as well as with the Declaration of Helsinki for human beings. The Human Development Index according to the United Nations Development Program (12) highlighted that, for 2012, in Colombia was 0.719 and, according to Global Data Lab (13), for Bogotá was 0.773.

Techniques and Procedures

Height was measured at the school facilities during school hours (Monday to Friday) during the month of October 2013. Date of birth information (day, month, and year) was requested from the school administration. The date of the evaluation was recorded, and with both records, the decimal age was obtained.

The height evaluation was carried out according to the suggestions described by Ross and Marfell-Jones (14). The procedure consisted of measuring height (cm) without shoes and with as little clothing as possible (only a light T-shirt and shorts). A portable stadiometer (Seca Gmbh & Co. KG, Hamburg, Germany) with an accuracy of 0.1 cm, according to the Frankfort plane, was used. To guarantee the technical error of stature measurement, it was measured twice, reflecting intra- and inter-observer values from R = .85 to.92.

The Z-score was calculated for each age and sex according to the standards described by the World Health Organization (15). The 1PB (9) nonlinear regression model 1 was used to infer the mathematical and biological parameters of height growth velocity and growth spurt for both sexes.

Statistics

Normality of data was verified by the Kolmogorov–Smirnov (K-S) test. After conforming to normality, descriptive statistics (mean, standard deviation, range) were calculated. Differences between both sexes were verified by means of the t-test for independent samples. To estimate the mathematical and biological parameters, the 1PB model was used. Five parameters were calculated according to the following equation:

h=h12(h1hθ)es0(tθ)+es1(tθ)

Here, h1: final height (cm), hθ and θ: average height (cm) and age (years) for height on the decreasing slope of the PHV, s0 and s1: prepubertal and pubertal rate constants controlling growth rate (cm/y). The calculations and graphs of the curves were obtained by means of the computer program implemented in the software R.

Results

The X ± SD values of heights of children and adolescents aligned by age and sex are shown in Table 1. There were no significant differences between both sexes from 5 to 8 years old and at 12 and 13 years old although, from 9 to 11 years old and 14 to 18 years old, the differences are significant (p <.05). The Z -score values in boys ranged from 0.20 to -0.82 cm and in girls from 0.32 to -0.78 cm. The height growth curve from 5 to 18 years of age for both sexes is observed in Figure 1. A similar growth pattern is observed until 8 years of age; then, from 9 to 11 years of age, girls showed greater height than boys (p <.05), and from 14 to 18 years of age, boys evidenced greater height than girls (p <.05).

TABLE 1
www.frontiersin.org

Table 1 Descriptive values (mean ± SD) and Z-score of the height of children and adolescents in Colombia.

FIGURE 1
www.frontiersin.org

Figure 1 Height growth curve of children and adolescents by age and sex.

The mathematical and biological parameters of the height of Colombian children and adolescents are shown in Table 2. The five mathematical parameters estimated by the 1PB model in general have reflected quality in the fit to the model, being the residual small (residual SE) in both sexes (0.241 in male and 0.203 in female). Final height (hi) (170.849 ± 0.434 cm) and peak height velocity size (hθ) (156.817 ± 0.495 cm) of boys were significantly higher relative to girls (hi = 157.934 ± 0.211 cm) and (hθ = 145.691 ± 0.863 cm) (p <.05).

TABLE 2
www.frontiersin.org

Table 2 Mathematical and biological parameters of stature, estimated by 1Preece-Baines (1PB) model.

In boys, the APHV was estimated at 12.708 ± 0.131 years, and in girls it was at 10.422 ± 0.195 years. In both ages, there were significant differences (p <.05). Girls reached APHV 2.23 years earlier than boys. In relation to PHV (cm/y), boys reached higher growth velocity in height, which was 7.430 ± 0.419 cm/y; however, in girls, it was 7.006 ± 0.186 cm/y. These values of APHV and PHV can be seen in Figure 2.

FIGURE 2
www.frontiersin.org

Figure 2 Peak height velocity curves of Colombian children and adolescents of both sexes.

Discussion

The results of the study evidence that schoolchildren living at moderate altitude in Bogotá (Colombia) reflect a final height in boys of 170.84 ± 0.43 cm and in girls of 157.93 ± 0.21 cm. These values are relatively similar to those reported by a recent study conducted in Colombia by Durán et al. (16) from birth to 20 years of age (in which, for boys, it was 172.3 cm and 159.4 cm for girls), covering cities such as Bogotá, Medellín, Cali, and Barranquilla that represent 92% of the Colombian population. In fact, Meisel-Roca et al. (17) highlight that disparities in average height between departments in Colombia were reduced in recent years, and the gap between regions has been closing throughout the century, especially due to the positive evolution of height during the period 1965–1990 when several ethnic groups in Colombia increased their height positively (18).

In relation to international studies, the final heights observed in our study are relatively similar to those reported in a cross-sectional study in Argentine children (19) and in British children through a longitudinal study (20) although Peruvian children and adolescents (8) reflect lower heights than those reported in this study (164.24 ± 0.67 cm in boys and 153.06 ± 0.29 cm in girls).

Regarding APHV, this study reports that children in Bogotá reflect 12.71 ± 0.13 y in boys and 10.42 ± 0.19 y in girls; i.e., these values presented prematurely (~1.6 years) earlier than indicated by the literature, in which the peak is reached around 14 years in boys and 12 years in girls approximately (11, 21).

The values observed in this study show earlier ages for APHV with respect to the study conducted in Yopal (Colombia), reporting 11.1 y in girls and 13.6 y in boys (22). On the other hand, when compared with international research, the results of this study are similar to those described in Chinese (4), Peruvian (8), and Taiwanese (23) children, in studies that used the 1BP model to estimate APHV in cross-sectional samples. Indeed, in all three studies, girls evidenced APHVs 2 years earlier than boys as observed in this study and the literature, respectively (11, 21).

In general, the estimation of APHVs cross-sectionally in the children in our study and in the Chinese, Peruvians, and Taiwanese children occurred prematurely, suggesting that values obtained in cross-sectional samples may underestimate APHVs. In fact, these divergences generally occur in cross-sectional samples, especially at puberty, when the shape of the underlying individual mean “growth” curve defines temporal changes in the timing of the cross-sectional distribution, whose data distribution may be transiently skewed (24).

On the other hand, PHV was higher in boys from Bogotá (7.43 ± 0.42 y) than girls from the same region (7.00 ± 0.19 y). These velocity patterns (cm/y) were more accelerated than similar ones from Yopal (Colombia) evidencing 6.96 cm/y in boys and 6.57 cm/y in girls (22). However, when compared with international research, some studies report values similar to our findings, such as, for example, those evidenced by Chinese (4) and Japanese (25) children, although some others have described height velocity higher than 7.5 cm/y in girls and 8.2 cm/y in Guatemalan and British children (20, 26), respectively.

Consequently, the cross-sectional studies using the 1PB model described above and the results obtained in this study report much lower velocities than those described in longitudinal studies (5, 11). These results are possibly due to some complications that cross-sectional studies usually present. For example, it is necessary to estimate derivatives (velocity and acceleration) from height measurements (27), which possibly the 1PB model could incur in a lower estimation of the velocity at peak stretch in relation to the models used in longitudinal studies (19, 20). However, it is also possible that cross-sectional studies show different cohorts in each of their ages, which could be exposed to different environmental conditions, which could force the model to adjust the data, consequently producing biases in the results (20).

In essence, in this study, we verified that final statures among adolescents differ with other study samples, including APHV and PHV varying between regions, so these findings confirm variations in physical growth potential between populations, which is determined by intergenerational factors—not only by genes transmitted to generations, but also to environmental living conditions (18).

The results of this study are relevant because, during the last century, the evolution of the biological standard of living in Colombia was a success story from the point of view of the secular increase in height and the reduction of socioeconomic inequality (28), including the increase in the human development index in recent years (13), all of which could be factors that explain in part the PHV reached prematurely and the reduction of disparities in final height compared to other populations.

Overall, despite the reduction of physical growth differences in Latin American regions and the improvement of living conditions, it remains to date a major public health problem as 5.1 million stunted affected children have been evidenced up to 2017 (29). In addition, data on physical growth and pubertal growth spurt parameters of children and adolescents in these regions remain scarce, so future studies should focus their research on three ethnic groups, namely indigenous, Afro-descendants, and Europeans with considerable degrees of miscegenation (30) as well as including Colombian children and adolescents living at sea level, at moderate altitude, and in tropical regions. This information may be useful to professionals and researchers working in auxology in general.

The study presents some strengths, for example, to our knowledge, this is the first cross-sectional study that was conducted in Bogotá (Colombia) on a large scale, estimating final height, APHVs, and PHVs in children and adolescents, as the results obtained provide relevant information to professionals working in clinical and epidemiological contexts. In addition, the biological parameters obtained can serve as a reference to compare with other regions, verify secular changes, and explore the timing of puberty among boys and girls, respectively.

Nevertheless, it was not possible to evaluate socioeconomic variables of the sample studied; however, it is assumed that children studying in Colombian state schools generally belong to a middle socioeconomic condition. Also, the selection of the nonprobabilistic sample does not allow generalizing the data to other contexts, and the 1PB model could underestimate the biological parameters, especially if cross-sectional data (20) such as in the present study are analyzed. Therefore, it is recommended that future studies should take these aspects into account and should be analyzed with caution.

In conclusion, a cross-sectional study was conducted on a large sample size of children living in Bogotá (Colombia) to determine growth patterns adjusted by the 1PB model. It was determined that final height size was reached at 170.84 ± 0.43 cm in boys and 157.93 ± 0.21 cm in girls, and APHV and PHV (cm/y) were reached relatively early in life and at average peak velocities similar to Asian and Western populations. A large-scale longitudinal study is needed to confirm these findings.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Ethics Statement

The studies involving human participants were reviewed and approved by Technological and Pedagogical University of Colombia. Written informed consent to participate in this study was provided by the participants’ legal guardian/next of kin.

Author Contributions

RG-C, MC-B, and RV-E conceived and designed the experiments. ED-B and CT-G performed the experiments. JM-N, MC-B, RG-C, PO, LU-A, and FC-C analyzed the data. MC-B, RG-C, RV-E, JF-L, and LS-M wrote, reviewed, and edited the paper. All authors contributed to the article and approved the submitted version.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

1. Tanner JM. Normal Growth and Techniques of Growth Assessment. Clin Endocrinol Metab (1986) 15(3):411–51. doi: 10.1016/S0300-595X(86)80005-6

PubMed Abstract | CrossRef Full Text | Google Scholar

2. Aßmann C, Hermanussen M. Modeling Determinants of Growth: Evidence for a Community-Based Target in Height? Pediatr Res (2013) 74:88–95. doi: 10.1038/pr.2013.50

PubMed Abstract | CrossRef Full Text | Google Scholar

3. Ulijaszek SJ. The International Growth Standard for Children and Adolescents Project: Environmental Influences on Preadolescent and Adolescent Growth in Weight and Height. Food Nutr Bulletin (2006) 27(4_suppl5):S279–94. doi: 10.1177/15648265060274S510

CrossRef Full Text | Google Scholar

4. Mao SH, Li HB, Jiang J, Sun X, Cheng JC, Qiu Y. An Updated Analysis of Pubertal Linear Growth Characteristics and Age at Menarche in Ethnic Chinese. Am J Hum Biol (2011) 23(1):132–7. doi: 10.1002/ajhb.21116

PubMed Abstract | CrossRef Full Text | Google Scholar

5. Tanner JM, Davies PS. Clinical Longitudinal Standards for Height and Height Velocity for North American Children. J Pediatr (1985) 107:317–29. doi: 10.1016/S0022-3476(85)80501-1

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Caruana EJ, Roman M, Hernández-Sánchez J, Solli P. Longitudinal Studies. J thoracic Dis (2015) 7(11):E537–40. doi: 10.3978/j.issn.2072-1439.2015.10.63

CrossRef Full Text | Google Scholar

7. Banik SD, Salehabadi SM, Dickinson F. Preece-Baines Model 1 to Estimate Height and Knee Height Growth in Boys and Girls From Merida, Mexico. Food Nutr Bull (2017) 38(2):182–95. doi: 10.1177/0379572117700270

PubMed Abstract | CrossRef Full Text | Google Scholar

8. Santos C, Bustamante A, Katzmarzyk PT, Vasconcelos O, Garganta R, Freitas D, et al. Growth Velocity Curves and Pubertal Spurt Parameters of Peruvian Children and Adolescents Living at Different Altitudes. The Peruvian Health and Optimist Growth Study. Am J Hum Biol (2019) 31(6):e23301. doi: 10.1002/ajhb.23301

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Preece M, Baines M. A New Family of Mathematical Models Describing the Human Growth Curve. Ann Hum Biol (1978) 5(1):1–24. doi: 10.1080/03014467800002601

PubMed Abstract | CrossRef Full Text | Google Scholar

10. Marshall WA, Tanner JM. Variations in Patterns of Pubertal Changes in Boys. Arch Dis Child (1970) 45:13–23. doi: 10.1136/adc.45.239.13

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Malina RM, Bouchard C, Bar-Or O. Growth Maturation and Physical Activity. ed 2. Champaign, IL: Human Kinetics Publihser, Inc. (2004).

Google Scholar

12. UNDP. Human Development Report 2013. The Rise of the South: Human Progress in a Diverse World. New York: UNDP (2013). Available at: http://hdr.undp.org/en/content/human-development-report-2013.

Google Scholar

13. Global Data Lab. Sub-National HDI - Subnational HDI (4.0). Global Data Lab. Netherlands: Institute for Management Research, Radboud University (2021).

Google Scholar

14. Ross, Marfell-Jones. Kinanthropometry. In: MacDougall JD, Wenger HA, Geeny HJ, editors. Physiological Testing of Elite Athlete. London: Human Kinetics (1991). p. p 223–30.

Google Scholar

15. WHO. WHO Child Growth Standards: Head Circumferencefor-Age, Arm Circumference-for- Age, Triceps Skinfold-for-Age and Subscapular Skinfold-for-Age: Methods and Development. WHO Library, Geneva: WHO (2007).

Google Scholar

16. Durán P, Merker A, Briceño G, Colón E, Line D, Abad V, et al. Colombian Reference Growth Curves for Height, Weight, Body Mass Index and Head Circumference. Acta Paediatr (2016) 105(3):e116–25. doi: 10.1111/apa.13269

PubMed Abstract | CrossRef Full Text | Google Scholar

17. Meisel-Roca A, Ramírez-Giraldo M, Santos-Cárdenas D. Socio-Economic Determinants and Spatial Converge of Biological Well-Being: The Casa of Colombia, 1920–1990. J Iberian Latin Am Economic History (2019) 37(2):297–338. doi: 10.1017/S0212610919000053

CrossRef Full Text | Google Scholar

18. Acosta K, Meisel A. Anthropometric Measurements by Ethnicity in Colombia, 1965-1990. Econ Hum Biol (2013) 11(4):416–25. doi: 10.1016/j.ehb.2013.03.006

PubMed Abstract | CrossRef Full Text | Google Scholar

19. Cuestas ME, Cieri ME, Ruiz Brünner MLM, Cuestas E. Height Growth Study of Healthy Children and Adolescents From Córdoba, Argentina. Rev Chil Pediatr (2020) 91(5):741–8. doi: 10.32641/rchped.v91i5.2066

PubMed Abstract | CrossRef Full Text | Google Scholar

20. Zemel BS, Johnston FE. Application of the Preece-Baines Growth Model to Cross-Sectional Data: Problems of Validity and Interpretation. Am J Hum Biol (1994) 6(5):563–70. doi: 10.1002/ajhb.1310060504

PubMed Abstract | CrossRef Full Text | Google Scholar

21. Tanner JM. Foetus Into Man: Physical Growth From Conception to Maturity. London, UK: Open Books Publishing Ltd. (1978).

Google Scholar

22. Ireton MJ, Carrillo JC, Caro LE. Biometry and Sexual Maturity in a Sample of Colombian Schoolchildren From El Yopal. Ann Hum Biol (2011) 38(1):39–52. doi: 10.3109/03014460.2010.487497

PubMed Abstract | CrossRef Full Text | Google Scholar

23. Lee TS, Chao T, Tang RB, Hsieh CC, Chen SJ, Ho LT. A Longitudinal Study of Growth Patterns in School Children in Taipei Area I: Growth Curve and Height Velocity Curve. Journal-Chinese Med Assoc (2004) 67(2):67–72.

Google Scholar

24. Cole TJ, Cortina-Borja M, Sandhu J, Kelly FP, Pan H. Nonlinear Growth Generates Age Changes in the Moments of the Frequency Distribution: The Example of Height in Puberty. Biostatistics (2008) 9(1):159–71. doi: 10.1093/biostatistics/kxm020

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Ali MA, Lestrel PE, Ohtsuki F. Adolescent Growth Events in Eight Decades of Japanese Cohort Data: Sex Differences. Am J Hum Biology: Off J Hum Biol Assoc (2001) 13(3):390–7. doi: 10.1002/ajhb.1063

CrossRef Full Text | Google Scholar

26. Bogin B, Wall M, MacVean RB. Longitudinal Analysis of Adolescent Growth of Ladino and Mayan School Children in Guatemala: Effects of Environment and Sex. Am J Phys Anthropol (1992) 89(4):447–57. doi: 10.1002/ajpa.1330890406

PubMed Abstract | CrossRef Full Text | Google Scholar

27. Ramsay J, Silverman B. Functional Data Analysis. 2 edn. New York: Springer-Verlag (2005). doi: 10.1007/b98888

CrossRef Full Text | Google Scholar

28. Meisel A, Vega M. The Biological Standard of Living (and its Convergence) in Colombia, 1870-2003. A Tropical Success Story. Econ Hum Biol (2007) 5(1):100–22. doi: 10.1016/j.ehb.2006.10.004

PubMed Abstract | CrossRef Full Text | Google Scholar

29. UNICEF (United Nations Children’s fund), WHO (World Health Organization), Bank W. Levels and Trends in Child Nutrition. New York: World Bank (2018).

Google Scholar

30. Gatica-Domínguez G, Mesenburg MA, Barros AJD, Victoria CG. Ethnic Inequalities in Child Stunting and Feeding Practices: Results From Surveys in Thirteen Countries From Latin America. Int J Equity Health (2020) 19:53. doi: 10.1186/s12939-020-01165-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: growth velocity, stature, final height, Preece–Baines function, children

Citation: Cossio-Bolaños MA, Vidal-Espinoza R, Minango-Negrete J, Olivares PR, Urzua-Alul L, de Campos LFCC, Fuentes-López J, Sanchez-Macedo L, Diaz-Bonilla E, Torres-Galvis C and Gomez-Campos R (2021) Estimation of Pubertal Growth Spurt Parameters in Children and Adolescents Living at Moderate Altitude in Colombia. Front. Endocrinol. 12:718292. doi: 10.3389/fendo.2021.718292

Received: 31 May 2021; Accepted: 01 July 2021;
Published: 08 September 2021.

Edited by:

George Paltoglou, National and Kapodistrian University of Athens, Greece

Reviewed by:

Tim Cole, University College London, United Kingdom
Dimitrios Papadimitriou, Athens Medical Center, Greece

Copyright © 2021 Cossio-Bolaños, Vidal-Espinoza, Minango-Negrete, Olivares, Urzua-Alul, de Campos, Fuentes-López, Sanchez-Macedo, Diaz-Bonilla, Torres-Galvis and Gomez-Campos. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Rossana Gomez-Campos, rossaunicamp@gmail.com

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.