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Received: 26 November 2019 Revised: 10 January 2020 Accepted: 19 January 2020 DOI: 10.1111/obr.13005 PEDIATRICS/PHYSIOLOGY Adipokines: A gear shift in puberty Desirée Nieuwenhuis | Natàlia Pujol-Gualdo Amanda J. Kiliaan Department of Anatomy, Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Preclinical Imaging Center PRIME, Nijmegen, The Netherlands Correspondence Amanda J. Kiliaan, PhD, Associate Professor, Department of Anatomy, Donders Institute for Brain, Cognition, and Behaviour, Preclinical Imaging Center PRIME, Radboud university medical center, 6500 HB Nijmegen, Geert Grooteplein 21N 6525 EZ Nijmegen, The Netherlands. Email: amanda.kiliaan@radboudumc.nl Funding information Europees Fonds voor Regionale Ontwikkeling (EFRO), Grant/Award Number: BriteN 2016 1 | INTRODUCTION The prevalence of obesity in adolescents and children is increasing in | Ilse A.C. Arnoldussen | Summary In this review, we discuss the role of adipokines in the onset of puberty in children with obesity during adrenarche and gonadarche and provide a clear and detailed overview of the biological processes of two major players, leptin and adiponectin. Adipokines, especially leptin and adiponectin, seem to induce an early onset of puberty in girls and boys with obesity by affecting the hypothalamic-pituitary- gonadal (HPG) axis. Moreover, adipokines and their receptors are expressed in the gonads, suggesting a role in sexual maturation and reproduction. All in all, adipokines may be a clue in understanding mechanisms underlying the onset of puberty in child- hood obesity and puberty onset variability. KEYWORDS adipokines, obesity, puberty 1,2 the age of 5 years were overweight or were with obesity in 2016, and 3 Obesity is defined by an excessive accumulation of white adipose tissue (WAT), and it is often indicated by a body mass index (BMI) 4 above 30. Two main types of adipose tissue were described: WAT and brown adipose tissue (BAT), which differ in morphology and func- 5-7 Ilse A.C. Arnoldussen and Amanda J. Kiliaan contributed equally to this work. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Obesity Reviews published by John Wiley & Sons Ltd on behalf of World Obesity Federation Obesity Reviews. 2020;21:e13005. wileyonlinelibrary.com/journal/obr 1 of 10 https://doi.org/10.1111/obr.13005 alarming rates. Specifically, worldwide, 41 million children below this number is expected to increase to 70 million in 2025. obesity is associated with various severe health complications, includ- ing increased risk of diabetes mellitus type 2, hypertension, heart dis- eases, and disturbances in sex hormone levels. 5,6 and mitochondria and plays a role in thermogenesis. Adipocytes in tion. BAT consists of adipocytes containing multiple lipid droplets WAT contain only a few mitochondria and a single lipid droplet. Adipose tissue has several functions including the storage of energy, thermogenesis, and the production and secretion of adipokines Generally, two physiological processes, adrenarche and gonadarche, 11,24 Childhood 5,7,8 a key role in puberty onset. Puberty is known as a period through which the body changes physically, being a physiological process resulting in the maturation of children, i.e. they develop sexual characteristics and obtain reproduc- 9,11 Adipokines are involved in a number of physiological processes including blood pressure, metabo- lism, glucose, and vascular homeostasis and may play amongst others 8-10 (hormones, cytokines, and peptides). tive functions. between obesity and puberty,2,12-23 the biological mechanisms under- lying obesity and puberty onset remain unclear. Hereafter, we review in detail the role of adipokines in the onset of puberty in childhood obesity. Although many studies have shown associations 2 | INITIATION OF PUBERTY PHYSIOLOGICAL PROCESSES IN THE interact to regulate the onset of puberty. During adrenarche, the adrenal cortex secretes steroid hormones (including 2 of 10 NIEUWENHUIS ET AL. androstenedione, dehydroepiandrosterone, dehydroepiandrosterone sulfate (DHEAS), androstenedione, and cortisol), insulin-like growth factor, and growth hormone, which contribute to the pubertal insights on new genetic loci (e.g. melanocortin-4 receptor, mitochon- drial carrier 2, and mitogen-activated protein kinase 13) and on sev- eral pathways that regulate the timing of puberty; however, it partly 34 9,24,25 Both adrenarche and gonadarche are involved in the development growth spurt, body odor, skin oiliness, and skeletal maturation. explains puberty timing variation. Thereby, defining the role of 25 adipokines is of importance in elucidating the variability in puberty as the expression of adipokines is sex-specific and is altered with body composition, adiposity, and during growth spurts. Moreover, adipokines and their receptors are expressed in gonads and several brain regions suggesting involvement in the onset of puberty and sex- ual maturation. Lastly, adipokines interfere in processes regulating timing and duration of puberty, for instance in the HPA and HPG axes which are both key players during adrenarche and gonadarche. Involvement of adipokines in the onset of puberty and specifically in individuals with obesity will be further reviewed in the next 2,24 3 | Puberty onset in girls is assessed using different markers, such as thelarche (breast development), menarche (the start of of pubic hair. pituitary-gonadal (HPG) axis is activated,2,26 and several hormones have been identified to participate in the activation of the HPG axis During gonadarche (Figure 1), the hypothalamic- 2,27 Kisspeptin, neurokinin B, and dynorphin are released by specialized including kisspeptin, neurokinin B, dynorphin, leptin, and ghrelin. 28 key regulator of the pulsatile secretion of gonadotropin releasing neurons, the KNDy neurons in the hypothalamus. Kisspeptin is a 29,30 B stimulates, and dynorphin inhibits the release of kisspeptin, which hormone (GnRH) from the hypothalamus. In addition, neurokinin implies that both coordinate a pulsatile release of kisspeptin. 31 Sub- sections. sequently, the activated HPG axis induces the pituitary gland to secrete luteinising hormone (LH) and follicle stimulating hormone (FSH). As a result, gametogenesis occurs, and the gonads will release sex hormones. Consequently, secondary sex characteristics develop including breast development in girls and an increased testicular vol- 2,26,32 is possibly due to differences in levels of body fat, hypothalamic-pitui- THE ONSET OF PUBERTY IN GIRLS ume in boys. The age at puberty onset varies greatly among individuals, which 19 35 menstruation), and pubic hair development. 33 genome-wide association studies have provided important new tary-adrenal (HPA) axis activity, and genetic background. Recent The average age of However, this age differs between cultures and ethnicities, and since 1980, age at menarche is girls at start of menarche is 12.4 years. 36 significantly decreasing. 36-39 F I G U R E 1 Hormonal regulation in the initiation of puberty in boys and girls. The secretion of kisspeptin, neurokinin B, and dynorphin from KNDy neurons initiate the release of gonadotropin releasing hormone (GnRH) from the hypothalamus. This activates the pituitary gland to produce and secrete luteinising hormone (LH) and follicle stimulating hormone (FSH), which in turn stimulate the gonads to produce estrogen and testosterone in girls and boys, respectively 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 3 of 10 T A B L E 1 Summary of included studies Authors Year Country Study Design Primary Outcome Sex Sample Size (n) Age (y) Data Collection Lian et al21 2019 China Cross-sectional Puberty starts earlier in Chinese Han girls with obesity compared with Chinese Han girls with normal weight. Girls 2996 9-19 2012 and 2013 Biro et al12 Lazzeri et al20 2018 USA 2018 Italy Longitudinal Cross-sectional Body mass index had a greater effect on age at menarche than did race and ethnicity. Girls 946 6-16 2004-2014 Li et al23 2018 China Longitudinal For both, boys and girls, a higher BMI (ie, overweight and obese) is associated with earlier onset of puberty Girls Girls Boys Girls 542 Deng et al22 Flom et al15 2017 China Cross-sectional Increased BMI is associated with early timing spermarche and menarche. Boys Girls Girls 1278258 9-15 2005-2012 He et al24 Holmgren et al17 2017 China 2017 Sweden Cross-sectional Longitudinal Onset of puberty is not related to obesity in boys. Boys Boys Girls Girls 782 7-17 972 929 5839 Kelly et al19 2017 UK 2016 Brazil 2016 USA Longitudinal prospective cohort Higher BMI in girls is associated with the onset of menstruation at an earlier age. 11 10-18 11-17 Barcellos Gemelli et al25 Cross-sectional Longitudinal Excess weight is associated with early age of menarche. Girls 727 2014 2003-2009 Glass et al16 Lee et al26 In girls, but not in boys, greater adiposity is associated with the earlier onset of puberty. Boys Girls 135 Cabrera et al27 Leonibus et al14 2014 USA 2013 Italy Cross-sectional Longitudinal Thelarche occurred earlier than recently reported, while age of menarche remained unchanged. Girls 610 3-17.9 2007 2005-2012 Currie et al13 2012 Europe, USA, Canada Cross-sectional Overweight/obesity during childhood predicts the early onset of puberty in girls. Girls 20410 11, 13, 15 2005-2006 2017 USA Prospective birth cohort Overweight/obese status at the age of 7 ye was associated with increased risk of early menarche 788 From birth to menarche occurred Pregnancies 1959-1966 2016 USA Cross-sectional Boys with overweight enter puberty earlier compared with boys with normal weight or obesity, while puberty starts later in boys with obesity compared with boys with normal weight and overweight. Boys 3872 6-16 2005-2010 Overweight during childhood shows a relation with the early onset of puberty in girls. 6535 4259 695 11 15 5.8-12.2 2009/2010 2013/2014 2014-2017 Higher BMI during childhood is associated with early puberty. 2008 and 2009 2000-2002 Obesity during childhood is related to the earlier onset of puberty. Boys Girls 84 123 71 (Continues) 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 4 of 10 NIEUWENHUIS ET AL. 3.1 | Fat storage For the initiation of puberty, the timing of stimulation and/or inhibi- tion of different hormones is important, and additionally, a certain amount and distribution of body fat is needed in order to start menar- che, which emphasizes the importance of body fat. From an evolution- ary point of view, body fat increases in mammalian females during puberty onset, and it highlights the need to guarantee a healthy preg- 40 women with anorexia nervosa. particularly body fat localized predominantly on the gluteofemoral fat depots, is profoundly associated with start of menarche, more than nancy, offspring, and maternal survival. fat, sex-hormones, and neuroendocrine alterations can evolve in men- strual dysfunction, for instance, in women with severe obesity or in 41-43 44-46 to gluteofemoral fat depots suggesting that leptin may convey infor- amount of total body fat. mation on body fat distribution to the hypothalamus during puberty. An improper level of body Importantly, body fat distribution, Blood leptin levels are strongly related 45 3.2 | HPG axis The HPG axis is activated by the release of kisspeptin resulting in the release of GnRH from the hypothalamus, and LH and FSH from the pituitary gland. In girls, FSH is involved in the development of the folli- cles in the ovaries, and it promotes the secretion of estrogen. LH stim- ulates the production of androgen hormones and induces ovulation 48 9,47 the release of kisspeptin and neurokinin B, and kisspeptin thereby (Figure 1). The secretion of estrogen has an inhibitory effect on inhibits the GnRH release from the hypothalamus. pattern of GnRH is important for the regulation of the menstrual cycle. This roughly 28-day-cycle comprises several phases, including the follicular phase and luteal phase. During the follicular phase, increasing levels of FSH stimulate the maturation of follicles and the production of estrogen from the ovaries. This in turn inhibits the release of FSH from the pituitary gland. A high level of estrogen will induce the production of LH by the pituitary gland, resulting in ovula- tion. The matured follicle secretes progesterone thereby inhibiting the release of GnRH. When the corpus luteum is demolished, there is less 48 3.3 | Adipokines According to results from studies reported in Table 1, girls with obe- sity enter puberty earlier compared with girls with normal higher leptin concentrations inhibit the intake of food and increases inhibition of GnRH. As a consequence, the cycle will start again. whole process, starting from the activated HPG axis, results in the development of the secondary sex characteristics in girls including 9,47 thelarche and menarche. 13,14,16-23,49-51 weight. these girls might be found in the secretion of adipokines. For instance, leptin is positively associated with the amount of body fat. Generally, energy expenditure. 9,52-54 An explanation for the early onset of puberty in The expression This TABLE 1 (Continued) Authors Year Country Study Design Primary Outcome Sample Sex Size (n) Age (y) Data Collection Herman-Giddens et al28 2012 USA Cross-sectional Observed mean ages of beginning genital and pubic hair growth and early testicular volumes were earlier than in past studies, depending on the characteristic and race/ethnicity. Boys 4131 6-16 2005-2010 Sorensen et al29 Aksglaede et al30 2010 2009 Denmark Denmark Cross-sectional/longitudinal Longitudinal Puberty onset at earlier ages was associated with an increased BMI in boys. Boys 1528 5.8-19.9 1991-1993/2006-2008 1930-1969 Juul et al31 Ribeiro et al32 2007 2006 Denmark Portugal Retrospective cohort Cross-sectional Higher BMI is associated with early voice break. 11-15 10-15 1990-1999 Kaplowitz et al18 Abbreviation: BMI, body mass USA Cross-sectional The early onset of puberty in Caucasian girls is likely related to an increased BMI. 5-12 1992-1993 2001 index. The higher BMI in boys and girls at 7 y of age, the earlier they enter puberty. Boys 21 612 Girls 135 223 Boys 463 Boys 382 Girls 437 Girls 10 750 Early sexual maturation in boys and girls is associated with overweight. 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 5 of 10 Leptin may possibly play a role in adrenarche as its plasma level increases with higher levels of body fat and as it can modulate both girls. 33 ing adrenarche. In coherence, in children with obesity, the androgen These findings suggested that lower reproductive status was associated with higher total adiponectin concentrations and that a higher reproductive status was related to higher HMW adiponectin the HPA and HPG axes. These axes are functionally integrated dur- DHEAS was positively associated with leptin levels. Nevertheless, concentrations in girls. In addition, individuals with obesity often another study showed that enhanced adrenal androgen secretion in girls with premature adrenarche was not explained by leptin or BMI 55 ated with androgen levels in girls ; however, it was not related to levels. and IL-6. TNF-α alters, and IL-6 inhibits the expression of 56 8 In addition, the adipokine adiponectin was negatively associ- 57 differences of adiponectin seem to develop during the progression of 56 adiponectin (Figure 2). Thereby, a low level of total adiponectin and/or high levels of inflammatory cytokines in individuals with obe- sity can promote the onset of puberty. Many more adipokines are secreted by WAT including omentin, 52,65-67 9,36,62,68 adrenarche in girls with Prader-Willi syndrome. Interestingly, sex puberty. adrenarche; however, both are not required factors. Thus, leptin and adiponectin might be able to influence In gonadarche, leptin can stimulate the secretion of kisspeptin, and subsequently activation of the HPG axis, which eventually increases the expression of estrogen and androstenedione in the ova- 58 2,60 65-67 The expression of these ries (Figure 2). Ob gene in WAT, resulting in the synthesis and secretion of leptin. Thus, high levels of leptin promote onset of puberty in girls via secre- tion of kisspeptin, and estrogen stimulates leptin secretion addition- ally. Moreover, adiponectin can affect the HPG axis due to the expression of adiponectin receptors in the hypothalamus, pituitary In return, estrogen stimulates the expression of the 59 gland, and gonads. onset as it inhibits the secretion of kisspeptin and GnRH in the hypo- thalamus and the release of GH and LH in the pituitary gland, and 2,60-62 52,60 63 girls with central precocious puberty (CPP). Moreover, total adiponectin had negative correlations with progression of puberty in girls (defined by Tanner stages), whereas HMW adiponectin had FIGURE 2 Adipokinesaffectingthe initiation of puberty in girls. Leptin stimulates the release of kisspeptin in KNDy neurons, which activates the hypothalamus to produce gonadotropin releasing hormone (GnRH). In response to the release of GnRH, the pituitary gland secretes follicle stimulating hormone (FSH) and luteinising hormone (LH), which stimulates the ovaries to release estrogen resulting in the formation of secondary sex characteristics in girls. Estrogen stimulates the production of leptin. Adiponectin inhibits GnRH release resulting in reduced levels of GnRH and thereby a delayed onset of puberty. TNF- α and IL-6 inhibit the production of adiponectin and therefore stimulate the onset of puberty In detail, adiponectin is a regulator of puberty thereby inhibiting the onset of puberty (Figure 2). with obesity often have low levels of adiponectin. et al. showed that total adiponectin was significantly lower, whereas high molecular weight (HMW) adiponectin was significantly higher in ment. 55 63 develop a chronic low-grade inflammatory state, which can be indi- cated by a high level of circulating inflammatory cytokines like TNF-α 64 Individuals Sitticharoon positive associations with LH levels and the progression of puberty in 63 visfatin, resistin, and chemerin. and visfatin are expressed in the ovaries. adipokines in the ovaries suggests a role within the reproductive sys- tem; however, the exact biological processes have to be examined. Thus, specifically leptin, adiponectin, and inflammatory cytokines pro- duced by WAT could be permissive key players during an early onset of puberty in girls with obesity. As an exception, HMW adiponectin seems to have a stimulatory effect on peripheral repro- ductive function as HMW is not able to cross the blood brain 63 barrier. 4 | Markers that are used to assess puberty onset in boys are THE ONSET OF PUBERTY IN BOYS spermarche, voice break, testicular volume, and pubic hair develop- 35 spermarche develop in the early stages of puberty onset, voice In women, omentin, chemerin, While pubic hair development, larger testicular volume, and 69 testicular volume increases, which occurs at an average age of break usually appears in later stages of puberty. Generally, first 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 6 of 10 NIEUWENHUIS ET AL. 11.9 years, followed by the development of pubic hair at 12.2 years of average, and lastly, boys experience spermarche around an aver- 55 related with leptin levels. Thereby, leptin plausibly has a minor impact in adrenarche in boys. Since leptin receptors are found in the hypothalamus, pituitary gland, and testes, they might be involved in the onset of puberty by affecting the HPG axis during gonadarche. Leptin stimulates the release of kisspeptin and GnRH, and as a consequence, it accelerates the onset of puberty (Table 1, Figure 3). In contrast, adiponectin inhibits the secretion of GnRH, GH, LH, and FSH therewith delaying the onset of puberty. However, adiponectin levels are generally lower in men compared with women and even lower in men with obe- age age of 13.4 years. 70 4.1 | Fat storage Many aspects of the reproductive physiology are energetically demanding,71 and therefore, an adequate energy level is necessary. In boys, a dynamic change in body composition occurs around the age of 10 to 13 years, in which they gain approximately 40% of sity. culating inflammatory cytokines. levels can stimulate the HPG axis and therewith an early onset of puberty in boys. Nevertheless, leptin can inhibit the production of tes- 72 mostly consisting of lean mass, which causes exhaustion of most of fat. Subsequently, a growth spurt follows in which they gain tissue 72 in boys, an adequate amount of body fat is important in the onset of their body fat. These alterations in amount of body fat indicate that 4.2 | Puberty in boys is initiated by the release of kisspeptin. As mentioned before, this activates the HPG axis, resulting in the release of GnRH from the hypothalamus, and consequently the release of LH and FSH 9,74 puberty. tosterone from the testes, to estrogen (Figure 3). of the development of secondary sex characteristics in boys. Additionally, leptin can affect fertility in men as it can modulate the nutritional support of spermatogenesis, and moreover, dysfunction of spermatogenesis is associated with an increased leptin level and 73 58 2,60-62 HPG axis from the pituitary gland (Figure 1). and LH stimulates the secretion of testosterone from the testes, which inhibits the release of kisspeptin from the KNDy neurons and 9,48 in men, the release of kisspeptin is more consistent, causing a con- 29,48 subsequently GnRH from the hypothalamus. receptors expressed on KNDy neurons. In humans, KNDy neurons Contrarily to women, LH-induced testosterone levels lead to the stant release of LH. development of secondary sex characteristics in boys. differences between sexes in kisspeptin release are related to a sex- specific and sex steroid-dependent kisspeptin system as estrogen and progesterone modulate kisspeptin activity through the sex-steroid 48 in the infundibular nucleus are involved in negative and positive sex- 48 tal exposure to sex steroids and result in sex-specific differences in steroid feedbacks. kisspeptin release. These sexual dimorphisms are induced by perina- 75,76 4.3 | Adipokines The association between obesity and puberty onset in boys is rather controversial compared with findings in girls. Most studies reported an early onset of puberty in boys associated with increased ate adipose tissue from actual breast tissue. stages are more difficult to assess than female stages as boys lack a more determined marker such as menarche. Thirdly, puberty onset can be indicated by the activation of the HPG axis, and the presence of these secondary sex characteristics is the result of hormonal 2 14,17,22,23,50,51,77,78 BMI, 20,49 all while others reported no associations at Current markers used 79 16,80 or a delayed onset of puberty (Table 1). The presence of excessive adipose tissue can be involved in puberty onset in boys as the secretion of adipokines can modulate both adrenarche and gonadarche. Leptin can affect adrenarche by modulating both the HPG and HPA axes,33 and moreover, androgen levels were positively 55 nal androgen secretion in boys with premature adrenarche was not associated with plasma leptin levels. Nevertheless, enhanced adre- 9 In more detail, 61,62 adiponectin, and individuals with obesity often have high levels of cir- Moreover, inflammatory cytokines, TNF-α, and IL-6, inhibit expression of the leptin receptor in the testis. FSH induces spermatogenesis, too. function and role still have to be examined. 64 High leptin and low adiponectin and fat tissue can convert testosterone Both processes might result in the delay 29,61,79 81,82 In men, other adipokines like chemerin are found in the gonads 65 Thus, particularly high leptin and low adiponectin levels stimulate the HPG axis and thereby accelerate the onset of puberty in boys. Additionally, leptin can dysregulate the development of secondary sex characteristics and spermatogenesis by affecting testosterone levels and nutritional sup- port of spermatogenesis. 5 | LIMITATIONS AND FUTURE RESEARCH DIRECTIONS Even though multiple epidemiological studies have shown the link between puberty onset and obesity, there are some important limita- tions. Firstly, determining both the onset and stage of puberty is rather difficult. For instance, assessing the stage of breast develop- ment in girls with obesity is complicated as clinicians should differenti- 2 changes in response to the activated HPG axis. to determine the onset of puberty refer to secondary sex characteris- tics, such as testicular volume in boys and breast development in girls. A more accurate measurement of puberty onset would be to combine secondary sex characteristics with plasma or serum hormone level measurements such as LH, FSH, adipokines, e.g. leptin. Thereby, differences in puberty measurements could explain variations in the age of puberty onset between boys and girls within different Thereby, resistin is expressed in the testes of rats, but its exact 83 Secondly, male pubertal 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 7 of 10 FIGURE 3 Adipokines affecting the initiation of puberty in boys. Leptin activates kisspeptin secretion in KNDy neurons, this activates the production of gonadotropin releasing hormone (GnRH) from the hypothalamus. GnRH stimulates the pituitary gland to secrete follicle stimulating hormone (FSH) and luteinising hormone (LH), activating the production of testosterone from the testes allowing the development of secondary sex characteristics. Leptin also inhibits the production of testosterone, which may cause a delayed onset of puberty. Adiponectin inhibits GnRH release. Low levels of adiponectin, as a result of TNF-α and IL-6 expression, lead to a reduced inhibition of GnRH. In response to GnRH release, the pituitary gland will secrete FSH and LH, and the testes will produce testosterone resulting in the development of secondary sex characteristics in boys countries, and In addition, the inclusion of a of puberty. ferent time points is complicated, as subjects examined several decades ago presented pronounced differences concerning lifestyle patterns such as nutrition and exercise habits. Lastly, obesity or over- weight is often determined by BMI, a classification based on weight and height measurements. Additionally, it is important that all studies studies or across continents, ethnicities proper age range (8-16 years) is important when assessing the onset (Figure 4). 12-15,17,20-23,49,77-79,84,85 30,47 Furthermore, comparison between studies from dif- 86 Specifically in children, BMI is often dependent on age and growth use the same anthropometric standards and sex-specific cut-offs. 13,14,16-23,49-51,77-80 fat and would represent a more accurate measurement in its regard. Based on this review, several suggestions can be made for further research. Firstly, the roles of adipokines like resistin, chemerin, visfatin, and omentin in puberty onset, fertility, and sexual maturation should be examined in detail. Secondly, future research examining the onset of puberty should combine indicators of puberty onset (e.g. breast development or testicular volume) with plasma or serum hor- mone measurements such as LH, FSH, sex-steroids, adipokines (e.g. spurts. ment in case of growth spurts. distribution of body fat should be taken into account in determining puberty and obesity in children. For instance, the body adiposity index (BAI), which was introduced in 2011 by Bergman et al.,87 uses hip cir- cumference and height in order to estimate the percentage of body 87 Thereby, BMI is a less accurate measure- F I G U R E 4 87,88 Therefore, both percentage and Average age of puberty onset in Europe, China, and the United States according to several studies from Table 1. Age of puberty onset ranges from 8.47 to 13.33 years in girls and from 8.63 leptin), and body fat distribution (e.g. BAI,87 waist-hip ratio's and/or dual-energy X-ray absorptiometry (DXA)2). Additionally, defining con- sistent and general measurements of puberty in both boys and girls, combined with a proper age range (8-16 years), would facilitate the comparisons between different studies and their results. 12-15, 17, 20-23, 25-29, 31 to 13.7 years in boys. included if average age of markers used to assess puberty was not reported. Pink: girls. Blue: boys Studies (Table 1) were not 39, 56 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 8 of 10 NIEUWENHUIS ET AL. 6 | CONCLUSION In conclusion, epidemiological data regarding obesity and puberty onset in girls show similar outcomes as adiposity results in the early onset of puberty in girls. 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Ann Epidemiol. 2017;27(3):187-93.e2. 16. Glass NA, Torner JC, Letuchy EM, et al. The relationship between greater prepubertal adiposity, subsequent age of maturation, and bone strength during adolescence. Journal of bone and mineral research: the official journal of the American Society for Bone and Min- eral Research. 2016;31(7):1455-1465. 17. Holmgren A, Niklasson A, Nierop AF, et al. Pubertal height gain is inversely related to peak BMI in childhood. Pediatr Res. 2017;81(3): 448-454. 18. Kaplowitz PB, Slora EJ, Wasserman RC, Pedlow SE, Herman- Giddens ME. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics. 2001;108(2):347-353. 19. Kelly Y, Zilanawala A, Sacker A, Hiatt R, Viner R. Early puberty in 11-year-old girls: Millennium Cohort Study findings. Arch Dis Child. 2017;102(3):232-237. 20. Lazzeri G, Tosti C, Pammolli A, et al. Overweight and lower age at menarche: evidence from the Italian HBSC cross-sectional survey. BMC Womens Health. 2018;18(1):168-174. thereby an early onset of obesity. leptin can inhibit the production of testosterone in boys and subse- quently inhibit the development of secondary sex characteristics affecting spermatogenesis. for other adipokines, like resistin and omentin, are present in the testes and ovaries suggesting a role in puberty or reproduction; 58, 71 however, their plausible function is still unknown. that adipokines may be key regulators in an early onset of puberty in both girls and boys with obesity, specifically by affecting the HPG axis during gonadarche. Future research should focus on assessing puberty onset by measuring consistent puberty markers and determine the percentage of body fat and its distribution and adipokines and hormone serum levels particularly involved in the HPG axis. CONFLICTS OF INTEREST The authors declare no conflict of interest. FUNDING INFORMATION This research was funded by Europees Fonds voor Regionale Ontwikkeling (EFRO), project BriteN 2016. ORCID Ilse A.C. Arnoldussen Amanda J. Kiliaan https://orcid.org/0000-0002-7395-5284 https://orcid.org/0000-0002-2158-6210 13, 14, 16-26, 29-32 Furthermore, several receptors Nevertheless, We conclude Search strategy We searched PubMed for articles published before Novem- ber 15th, 2019 using relevant keywords, including ‘onset of puberty and adiposity/obesity’, ‘onset of puberty’, ‘children with obesity’, ‘adipose tissue’, ‘childhood obesity’, ‘adiposity’, ‘obesity’, ‘adipokine(s)’, ‘HPG axis’, ‘adipokines ovary/ova- ries’, or ‘adipokines testes’, either alone or in combination. Selection criteria used were English language, longitudinal or cross-sectional studies assessing the onset of puberty, including menarche, thelarche, spermarche, or voice break, combined with high BMI or obesity/adiposity, and articles assessing or reviewing adipokines and its effects on the reproductive system. 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License NIEUWENHUIS ET AL. 9 of 10 21. Lian Q, Mao Y, Luo S, et al. Puberty timing associated with obesity and central obesity in Chinese Han girls. BMC Pediatr. 2019; 19(1):1-7. 22. Deng Y, Liang J, Zong Y, et al. Timing of spermarche and menarche among urban students in Guangzhou, China: trends from 2005 to 2012 and association with Obesity. 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Trends in menarcheal age between 1955 and 2009 in the Netherlands. PLoS ONE. 2013;8:e60056-e60056. 40. Kaplan HS, Lancaster JB. An evolutionary and ecological analysis of human fertility, mating patterns, and parental investment. Off- spring: Human fertility behavior in biodemographic perspective. 2003;1: 170-223. 41. Mitan LA. Menstrual dysfunction in anorexia nervosa. J Pediatr Adolesc Gynecol. 2004;17(2):81-85. 42. Xu H, Li P-H, Barrow TM, et al. Obesity as an effect modifier of the association between menstrual abnormalities and hypertension in young adult women: Results from Project ELEFANT. PLoS ONE. 2018; 13(11):e0207929-e0207929. 43. Tauqeer Z, Gomez G, Stanford FC. Obesity in women: insights for the clinician. J Womens Health (Larchmt). 2018;27(4):444-457. 44. de Ridder CM, Thijssen JH, Bruning PF, Van den Brande JL, Zonderland ML, Erich WB. Body fat mass, body fat distribution, and pubertal development: a longitudinal study of physical and hormonal sexual maturation of girls. J Clin Endocrinol Metab. 1992;75(2): 442-446. 45. Lassek W, Gaulin S. Brief communication: menarche is related to fat distribution. Am J Phys Anthropol. 2007;133(4):1147-1151. 46. Loomba-Albrecht LA, Styne DM. Effect of puberty on body composi- tion. Curr Opin Endocrinol Diabetes Obes. 2009;16:10-15. 47. Simonneaux V, Bahougne T. A multi-oscillatory circadian system times female reproduction. Front Endocrinol. 2015;6:1-15. 48. Marques P, Skorupskaite K, George JT, Anderson RA. Physiology of GNRH and gonadotropin secretion. In: Feingold KR, Anawalt B, Boyce A, et al., eds. Endotext. Endotext.org: South Dartmouth (MA); 2000. 49. Barcellos Gemelli IF, Farias EDS, Souza OF. Age at menarche and its association with excess weight and body fat percentage in girls in the Southwestern Region of the Brazilian Amazon. 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Obesity Reviews. 2020;21:e13005. https://doi.org/ 10.1111/obr.13005 1467789x, 2020, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/obr.13005, Wiley Online Library on [10/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are goverILLINOIS PROFESSIONAL TEACHING STANDARDS (2013) Standard 1 - Teaching Diverse Students – The competent teacher understands the diverse characteristics and abilities of each student and how individuals develop and learn within the context of their social, economic, cultural, linguistic, and academic experiences. The teacher uses these experiences to create instructional opportunities that maximize student learning. Knowledge Indicators – The competent teacher: 1A) understands the spectrum of student diversity (e.g., race and ethnicity, socioeconomic status, special education, gifted, English language learners (ELL), sexual orientation, gender, gender identity) and the assets that each student brings to learning across the curriculum; 1B) understands how each student constructs knowledge, acquires skills, and develops effective and efficient critical thinking and problem-solving capabilities; 1C) understands how teaching and student learning are influenced by development (physical, social and emotional, cognitive, linguistic), past experiences, talents, prior knowledge, economic circumstances and diversity within the community; 1D) understands the impact of cognitive, emotional, physical, and sensory disabilities on learning and communication pursuant to the Individuals with Disabilities Education Improvement Act (also referred to as “IDEA”) (20 USC 1400 et seq.), its implementing regulations (34 CFR 300; 2006), Article 14 of the School Code [105 ILCS 5/Art.14] and 23 Ill. Adm. Code 226 (Special Education); 1E) understands the impact of linguistic and cultural diversity on learning and communication; 1F) understands his or her personal perspectives and biases and their effects on one’s teaching; and 1G) understands how to identify individual needs and how to locate and access technology, services, and resources to address those needs. Performance Indicators – The competent teacher: 1H) analyzes and uses student information to design instruction that meets the diverse needs of students and leads to ongoing growth and achievement; 1I) stimulates prior knowledge and links new ideas to already familiar ideas and experiences; 1J) differentiates strategies, materials, pace, levels of complexity, and language to introduce concepts and principles so that they are meaningful to students at varying levels of development and to students with diverse learning needs; 1K) facilitates a learning community in which individual differences are respected; and 1L) uses information about students’ individual experiences, families, cultures, and communities to create meaningful learning opportunities and enrich instruction for all students. Standard 2 - Content Area and Pedagogical Knowledge – The competent teacher has in-depth understanding of content area knowledge that includes central concepts, methods of inquiry, structures of the disciplines, and content area literacy. The teacher creates meaningful learning experiences for each student based upon interactions among content area and pedagogical knowledge, and evidence-based practice. Knowledge Indicators – The competent teacher: 2A) understands theories and philosophies of learning and human development as they relate to the range of students in the classroom; 2B) understands major concepts, assumptions, debates, and principles; processes of inquiry; and theories that are central to the disciplines; 2C) understands the cognitive processes associated with various kinds of learning (e.g., critical and creative thinking, problem-structuring and problem-solving, invention, memorization, and recall) 2 and ensures attention to these learning processes so that students can master content standards; 2D) understands the relationship of knowledge within the disciplines to other content areas and to life applications; 2E) understands how diverse student characteristics and abilities affect processes of inquiry and influence patterns of learning; 2F) knows how to access the tools and knowledge related to latest findings (e.g., research, practice, methodologies) and technologies in the disciplines; 2G) understands the theory behind and the process for providing support to promote learning when concepts and skills are first being introduced; and 2H) understands the relationship among language acquisition (first and second), literacy development, and acquisition of academic content and skills. Performance Indicators – The competent teacher: 2I) evaluates teaching resources and materials for appropriateness as related to curricular content and each student’s needs; 2J) uses differing viewpoints, theories, and methods of inquiry in teaching subject matter concepts; 2K) engages students in the processes of critical thinking and inquiry and addresses standards of evidence of the disciplines; 2L) demonstrates fluency in technology systems, uses technology to support instruction and enhance student learning, and designs learning experiences to develop student skills in the application of technology appropriate to the disciplines; 2M) uses a variety of explanations and multiple representations of concepts that capture key ideas to help each student develop conceptual understanding and address common misunderstandings; 2N) facilitates learning experiences that make connections to other content areas and to life experiences; 2O) designs learning experiences and utilizes assistive technology and digital tools to provide access to general curricular content to individuals with disabilities; 2P) adjusts practice to meet the needs of each student in the content areas; and 2Q) applies and adapts an array of content area literacy strategies to make all subject matter accessible to each student. Standard 3 - Planning for Differentiated Instruction – The competent teacher plans and designs instruction based on content area knowledge, diverse student characteristics, student performance data, curriculum goals, and the community context. The teacher plans for ongoing student growth and achievement. Knowledge Indicators – The competent teacher: 3A) understands the Illinois Learning Standards (23 Ill. Adm. Code 1.Appendix D), curriculum development process, content, learning theory, assessment, and student development and knows how to incorporate this knowledge in planning differentiated instruction; 3B) understands how to develop short- and long-range plans, including transition plans, consistent with curriculum goals, student diversity, and learning theory; 3C) understands cultural, linguistic, cognitive, physical, and social and emotional differences, and considers the needs of each student when planning instruction; 3D) understands when and how to adjust plans based on outcome data, as well as student needs, goals, and responses; 3E) understands the appropriate role of technology, including assistive technology, to address student needs, as well as how to incorporate contemporary tools and resources to maximize student learning; 3 3F) understands how to co-plan with other classroom teachers, parents or guardians, paraprofessionals, school specialists, and community representatives to design learning experiences; and 3G) understands how research and data guide instructional planning, delivery, and adaptation. Performance Indicators – The competent teacher: 3H) establishes high expectations for each student’s learning and behavior; 3I) creates short-term and long-term plans to achieve the expectations for student learning; 3J) uses data to plan for differentiated instruction to allow for variations in individual learning needs; 3K) incorporates experiences into instructional practices that relate to a student’s current life experiences and to future life experiences; 3L) creates approaches to learning that are interdisciplinary and that integrate multiple content areas; 3M) develops plans based on student responses and provides for different pathways based on student needs; 3N) accesses and uses a wide range of information and instructional technologies to enhance a student’s ongoing growth and achievement; 3O) when planning instruction, addresses goals and objectives contained in plans developed under Section 504 of the Rehabilitation Act of 1973 (29 USC 794), individualized education programs (IEP) (see 23 Ill. Adm. Code 226 (Special Education)) or individual family service plans (IFSP) (see 23 Ill. Adm. Code 226 and 34 CFR 300.24; 2006); 3P) works with others to adapt and modify instruction to meet individual student needs; and 3Q) develops or selects relevant instructional content, materials, resources, and strategies (e.g., project-based learning) for differentiating instruction. Standard 4 - Learning Environment – The competent teacher structures a safe and healthy learning environment that facilitates cultural and linguistic responsiveness, emotional well-being, self-efficacy, positive social interaction, mutual respect, active engagement, academic risk-taking, self-motivation, and personal goal-setting. Knowledge Indicators – The competent teacher: 4A) understands principles of and strategies for effective classroom and behavior management; 4B) understands how individuals influence groups and how groups function in society; 4C) understands how to help students work cooperatively and productively in groups; 4D) understands factors (e.g., self-efficacy, positive social interaction) that influence motivation and engagement; 4E) knows how to assess the instructional environment to determine how best to meet a student’s individual needs; 4F) understands laws, rules, and ethical considerations regarding behavior intervention planning and behavior management (e.g., bullying, crisis intervention, physical restraint); 4G) knows strategies to implement behavior management and behavior intervention planning to ensure a safe and productive learning environment; and 4H) understands the use of student data (formative and summative) to design and implement behavior management strategies. Performance Indicators – The competent teacher: 4I) creates a safe and healthy environment that maximizes student learning; 4J) creates clear expectations and procedures for communication and behavior and a physical setting conducive to achieving classroom goals; 4K) uses strategies to create a smoothly functioning learning community in which students assume responsibility for themselves and one another, participate in decision-making, work collaboratively and independently, use appropriate technology, and engage in purposeful learning activities; 4 4L) analyzes the classroom environment and makes decisions to enhance cultural and linguistic responsiveness, mutual respect, positive social relationships, student motivation, and classroom engagement; 4M) organizes, allocates, and manages time, materials, technology, and physical space to provide active and equitable engagement of students in productive learning activities; 4N) engages students in and monitors individual and group-learning activities that help them develop the motivation to learn; 4O) uses a variety of effective behavioral management techniques appropriate to the needs of all students that include positive behavior interventions and supports; 4P) modifies the learning environment (including the schedule and physical arrangement) to facilitate appropriate behaviors and learning for students with diverse learning characteristics; and 4Q) analyzes student behavior data to develop and support positive behavior. Standard 5 - Instructional Delivery – The competent teacher differentiates instruction by using a variety of strategies that support critical and creative thinking, problem-solving, and continuous growth and learning. This teacher understands that the classroom is a dynamic environment requiring ongoing modification of instruction to enhance learning for each student. Knowledge Indicators – The competent teacher: 5A) understands the cognitive processes associated with various kinds of learning; 5B) understands principles and techniques, along with advantages and limitations, associated with a wide range of evidence-based instructional practices; 5C) knows how to implement effective differentiated instruction through the use of a wide variety of materials, technologies, and resources; 5D) understands disciplinary and interdisciplinary instructional approaches and how they relate to life and career experiences; 5E) knows techniques for modifying instructional methods, materials, and the environment to facilitate learning for students with diverse learning characteristics; 5F) knows strategies to maximize student attentiveness and engagement; 5G) knows how to evaluate and use student performance data to adjust instruction while teaching; and 5H) understands when and how to adapt or modify instruction based on outcome data, as well as student needs, goals, and responses. Performance Indicators – The competent teacher: 5I) uses multiple teaching strategies, including adjusted pacing and flexible grouping, to engage students in active learning opportunities that promote the development of critical and creative thinking, problem-solving, and performance capabilities; 5J) monitors and adjusts strategies in response to feedback from the student; 5K) varies his or her role in the instructional process as instructor, facilitator, coach, or audience in relation to the content and purposes of instruction and the needs of students; 5L) develops a variety of clear, accurate presentations and representations of concepts, using alternative explanations to assist students’ understanding and presenting diverse perspectives to encourage critical and creative thinking; 5M) uses strategies and techniques for facilitating meaningful inclusion of individuals with a range of abilities and experiences; 5N) uses technology to accomplish differentiated instructional objectives that enhance learning for each student; 5O) models and facilitates effective use of current and emerging digital tools to locate, analyze, evaluate, and use information resources to support research and learning; 5P) uses student data to adapt the curriculum and implement instructional strategies and materials according to the characteristics of each student; 5 5Q) uses effective co-planning and co-teaching techniques to deliver instruction to all students; 5R) maximizes instructional time (e.g., minimizes transitional time); and 5S) implements appropriate evidence-based instructional strategies. Standard 6 - Reading, Writing, and Oral Communication – The competent teacher has foundational knowledge of reading, writing, and oral communication within the content area and recognizes and addresses student reading, writing, and oral communication needs to facilitate the acquisition of content knowledge. Knowledge Indicators – The competent teacher: 6A) understands appropriate and varied instructional approaches used before, during, and after reading, including those that develop word knowledge, vocabulary, comprehension, fluency, and strategy use in the content areas; 6B) understands that the reading process involves the construction of meaning through the interactions of the reader's background knowledge and experiences, the information in the text, and the purpose of the reading situation; 6C) understands communication theory, language development, and the role of language in learning; 6D) understands writing processes and their importance to content learning; 6E) knows and models standard conventions of written and oral communications; 6F) recognizes the relationships among reading, writing, and oral communication and understands how to integrate these components to increase content learning; 6G) understands how to design, select, modify, and evaluate a wide range of materials for the content areas and the reading needs of the student; 6H) understands how to use a variety of formal and informal assessments to recognize and address the reading, writing, and oral communication needs of each student; and 6I) knows appropriate and varied instructional approaches, including those that develop word knowledge, vocabulary, comprehension, fluency, and strategy use in the content areas. Performance Indicators – The competent teacher: 6J) selects, modifies, and uses a wide range of printed, visual, or auditory materials, and online resources appropriate to the content areas and the reading needs and levels of each student (including ELLs, and struggling and advanced readers); 6K) uses assessment data, student work samples, and observations from continuous monitoring of student progress to plan and evaluate effective content area reading, writing, and oral communication instruction; 6L) facilitates the use of appropriate word identification and vocabulary strategies to develop each student’s understanding of content; 6M) teaches fluency strategies to facilitate comprehension of content; 6N) uses modeling, explanation, practice, and feedback to teach students to monitor and apply comprehension strategies independently, appropriate to the content learning; 6O) teaches students to analyze, evaluate, synthesize, and summarize information in single texts and across multiple texts, including electronic resources; 6P) teaches students to develop written text appropriate to the content areas that utilizes organization (e.g., compare/contrast, problem/solution), focus, elaboration, word choice, and standard conventions (e.g., punctuation, grammar); 6Q) integrates reading, writing, and oral communication to engage students in content learning; 6R) works with other teachers and support personnel to design, adjust, and modify instruction to meet students’ reading, writing, and oral communication needs; and 6S) stimulates discussion in the content areas for varied instructional and conversational purposes. Standard 7 - Assessment – The competent teacher understands and uses appropriate formative and summative assessments for determining student needs, monitoring student progress, measuring student 6 growth, and evaluating student outcomes. The teacher makes decisions driven by data about curricular and instructional effectiveness and adjusts practices to meet the needs of each student. Knowledge Indicators – The competent teacher: 7A) understands the purposes, characteristics, and limitations of different types of assessments, including standardized assessments, universal screening, curriculum-based assessment, and progress monitoring tools; 7B) understands that assessment is a means of evaluating how students learn and what they know and are able to do in order to meet the Illinois Learning Standards; 7C) understands measurement theory and assessment-related issues, such as validity, reliability, bias, and appropriate and accurate scoring; 7D) understands current terminology and procedures necessary for the appropriate analysis and interpretation of assessment data; 7E) understands how to select, construct, and use assessment strategies and instruments for diagnosis and evaluation of learning and instruction; 7F) knows research-based assessment strategies appropriate for each student; 7G) understands how to make data-driven decisions using assessment results to adjust practices to meet the needs of each student; 7H) knows legal provisions, rules, and guidelines regarding assessment and assessment accommodations for all student populations; and 7I) knows assessment and progress monitoring techniques to assess the effectiveness of instruction for each student. Performance Indicators – The competent teacher: 7J) uses assessment results to determine student performance levels, identify learning targets, select appropriate research-based instructional strategies, and implement instruction to enhance learning outcomes; 7K) appropriately uses a variety of formal and informal assessments to evaluate the understanding, progress, and performance of an individual student and the class as a whole; 7L) involves students in self-assessment activities to help them become aware of their strengths and needs and encourages them to establish goals for learning; 7M) maintains useful and accurate records of student work and performance; 7N) accurately interprets and clearly communicates aggregate student performance data to students, parents or guardians, colleagues, and the community in a manner that complies with the requirements of the Illinois School Student Records Act [105 ILCS 10], 23 Ill. Adm. Code 375 (Student Records), the Family Educational Rights and Privacy Act (FERPA) (20 USC 1232g) and its implementing regulations (34 CFR 99; December 9, 2008); 7O) effectively uses appropriate technologies to conduct assessments, monitor performance, and assess student progress; 7P) collaborates with families and other professionals involved in the assessment of each student; 7Q) uses various types of assessment procedures appropriately, including making accommodations for individual students in specific contexts; and 7R) uses assessment strategies and devices that are nondiscriminatory, and take into consideration the impact of disabilities, methods of communication, cultural background, and primary language on measuring knowledge and performance of students. Standard 8 - Collaborative Relationships – The competent teacher builds and maintains collaborative relationships to foster cognitive, linguistic, physical, and social and emotional development. This teacher works as a team member with professional colleagues, students, parents or guardians, and community members. Knowledge Indicators – The competent teacher: 8A) understands schools as organizations within the larger community context; 7 8B) understands the collaborative process and the skills necessary to initiate and carry out that process; 8C) collaborates with others in the use of data to design and implement effective school interventions that benefit all students; 8D) understands the benefits, barriers, and techniques involved in parent and family collaborations; 8E) understands school- and work-based learning environments and the need for collaboration with all organizations (e.g., businesses, community agencies, nonprofit organizations) to enhance student learning; 8F) understands the importance of participating on collaborative and problem-solving teams to create effective academic and behavioral interventions for all students; 8G) understands the various models of co-teaching and the procedures for implementing them across the curriculum; 8H) understands concerns of families of students with disabilities and knows appropriate strategies to collaborate with students and their families in addressing these concerns; and 8I) understands the roles and the importance of including students with disabilities, as appropriate, and all team members in planning individualized education programs (i.e, IEP, IFSP, Section 504 plan) for students with disabilities. Performance Indicators – The competent teacher: 8J) works with all school personnel (e.g., support staff, teachers, paraprofessionals) to develop learning climates for the school that encourage unity, support a sense of shared purpose, show trust in one another, and value individuals; 8K) participates in collaborative decision-making and problem-solving with colleagues and other professionals to achieve success for all students; 8L) initiates collaboration with others to create opportunities that enhance student learning; 8M) uses digital tools and resources to promote collaborative interactions; 8N) uses effective co-planning and co-teaching techniques to deliver instruction to each student; 8O) collaborates with school personnel in the implementation of appropriate assessment and instruction for designated students; 8P) develops professional relationships with parents and guardians that result in fair and equitable treatment of each student to support growth and learning; 8Q) establishes respectful and productive relationships with parents or guardians and seeks to develop cooperative partnerships to promote student learning and well-being; 8R) uses conflict resolution skills to enhance the effectiveness of collaboration and teamwork; 8S) participates in the design and implementation of individualized instruction for students with special needs (i.e., IEPs, IFSP, transition plans, Section 504 plans), ELLs, and students who are gifted; and 8T) identifies and utilizes community resources to enhance student learning and to provide opportunities for students to explore career opportunities. Standard 9 - Professionalism, Leadership, and Advocacy – The competent teacher is an ethical and reflective practitioner who exhibits professionalism; provides leadership in the learning community; and advocates for students, parents or guardians, and the profession. Knowledge Indicators – The competent teacher: 9A) evaluates best practices and research-based materials against benchmarks within the disciplines; 9B) knows laws and rules (e.g., mandatory reporting, sexual misconduct, corporal punishment) as a foundation for the fair and just treatment of all students and their families in the classroom and school; 9C) understands emergency response procedures as required under the School Safety Drill Act [105 ILCS 128/1], including school safety and crisis intervention protocol, initial response 8 actions (e.g., whether to stay in or evacuate a building), and first response to medical emergencies (e.g., first aid and life-saving techniques); 9D) identifies paths for continuous professional growth and improvement, including the design of a professional growth plan; 9E) is cognizant of his or her emerging and developed leadership skills and the applicability of those skills within a variety of learning communities; 9F) understands the roles of an advocate, the process of advocacy, and its place in combating or promoting certain school district practices affecting students; 9G) understands local and global societal issues and responsibilities in an evolving digital culture; and 9H) understands the importance of modeling appropriate dispositions in the classroom. Performance Indicators – The competent teacher: 9I) models professional behavior that reflects honesty, integrity, personal responsibility, confidentiality, altruism and respect; 9J) maintains accurate records, manages data effectively, and protects the confidentiality of information pertaining to each student and family; 9K) reflects on professional practice and resulting outcomes; engages in self-assessment; and adjusts practices to improve student performance, school goals, and professional growth; 9L) communicates with families, responds to concerns, and contributes to enhanced family participation in student education; 9M) communicates relevant information and ideas effectively to students, parents or guardians, and peers, using a variety of technology and digital-age media and formats; 9N) collaborates with other teachers, students, parents or guardians, specialists, administrators, and community partners to enhance students’ learning and school improvement; 9O) participates in professional development, professional organizations, and learning communities, and engages in peer coaching and mentoring activities to enhance personal growth and development; 9P) uses leadership skills that contribute to individual and collegial growth and development, school improvement, and the advancement of knowledge in the teaching profession; 9Q) proactively serves all students and their families with equity and honor and advocates on their behalf, ensuring the learning and well-being of each child in the classroom; 9R) is aware of and complies with the mandatory reporter provisions of Section 4 of the Abused and Neglected Child Reporting Act [325 ILCS 5/4]; 9S) models digital etiquette and responsible social actions in the use of digital technology; and 9T) models and teaches safe, legal, and ethical use of digital information and technology, including respect for copyright, intellectual property, and the appropriate documentation of sources.Integrated Music/English testSure! Here are the English words only: 1. Stage 2. Lighting effects 3. Live 4. Release 5. Focus on 6. Be inspired 7. Works of art 8. Exhibition 9. Art movement 10. Exhibit 11. Landscape painting 12. Cast 13. Full house 14. Be performed 15. Audience 16. Computer-generated imagery 17. Humanoid tribe 18. Apply 19. Virtual image 20. Box office hit 21. Motion capture techniques 22. Facial expression 23. Lifelike 24. Live action scene 25. Simulation camera 26. Absorb 27. Influence 28. Three-dimensional computer graphics 29. Animation 30. The media 31. Enhance 32. Visual effects 33. Special effects 34. Come along 35. Light year 36. Make a dream come true 37. Catch up to 38. Widely 39. Limitation 40. Animated characters 41. Marker 42. Reflector 43. Record 44. Realistic movement 45. Detailed 46. Human expression 47. Landscape 48. Full range 49. Develop 50. One-of-a-kind 51. Copy 52. Headgear 53. Equipped with 54. Muscle 55. Digital character 56. Truly 57. Authentic 58. Field of knowledge 59. Integrate with 60. Expert in 61. Surrounding 62. Take something a step further 63. Production stage 64. Fusion 65. Eyepiece 66. State-of-the-art technology 67. Interact 68. Aspect 69. Groundbreaking 70. Lead the wayTo the Lakota, and other indigenous people on North America's Great Plains, the bison was an essential part of their culture ( expressed in the quote on the previous page). The bison provided meat for nutrition, a hide for clothing and shelter, bones for tools, and fat for soap. The bison was also central to their religious beliefs. So, when European settlers hunted the bison nearly to extinction, Lakota culture suffered. Culture is central to a society and the identity of its people, as well as its continued existence. Therefore, geographers study culture as a way to understand similarities and differences among societies across the world, and in some cases, to help preserve these societies. Analyzing Culture All of a group's learned behaviors, actions, beliefs, and objects are a part of culture. It is a visible force seen in a group's actions, possessions, and influence on the landscape. For example, in a large city you can see people working in offices, factories, and stores, and living in high-rise apartments or suburban homes. You might observe them attending movies, concerts, or sporting events. Culture is also an invisible force guiding people through shared belief systems, customs, and traditions. Culture is learned, in that it develops through experiences, and not merely transmitted through genetics. For example, many people in the United States have developed a strong sense of competitiveness in school and business, and believe that hard work is a key to success. These types of elements, visible and invisible, are cultural traits. A series of interrelated traits make up a cultural complex, such as the process of steps and acceptable behaviors related to greeting a person in different cultures. A single cultural artifact, such as an automobile, may represent many different values, beliefs, behaviors and traditions and be representative of a cultural complex. Since culture is learned there are many ways that one generation passes its culture to the next. Children and adults learn traits three ways: • imitation, as when learning a language by repeating sounds or behaviors from a person or television • informal instruction, as when a parent reminds a child to say "please" • formal instruction, as when students learn history in school 132 HUMAN GEOGRAPHY: AP" EDITION CULTURAL COMPLEX OF THE AUTOMOBILE The automobile provides much more than just transportation, as it reflects many values that are central to American culture. Origins of Culture The area in which a unique culture or a specific trait develops is a culture hearth. Classical Greece was a culture hearth for democracy more than 2,000 years ago. New York City was a culture hearth for rap music in the 1970s. Geographers study how cultures develop in hearths and diffuse-or spread-to other places. Geographers also study taboos, behaviors heavily discouraged by a culture. For example, many cultures have taboos against eating certain foods, such as pork or insects. What is considered taboo changes over time. In the United States, marriages between Protestants and Catholics were once taboo, but they are not widely opposed now. Traditional, Folk, and Indigenous Cultures With the beginning of the Industrial Revolution in the late 18th century, modern transportation and communication connected people as never before and led to extensive cultural mixing, especially as cities have grown. The world prior to this time was very different; however, remnants of the past are still evident in our modern cultures. Traditional, folk, and indigenous cultures share some important characteristics and are often grouped together, but they do have some subtle differences. Traditional Culture Recently, the meanings of traditional, folk, and indigenous culture have begun to merge, causing geographers to debate when each should be used. Increasingly, the term traditional culture is used to encompass all three cultural designations. All three types share the function of passing down long-held beliefs, values, and practices and are generally resistant to rapid changes in their culture. Folk Culture The beliefs and practices of small, homogenous groups of people, often living in rural areas that are relatively isolated and slow to change, are known as folk cultures. Like all cultures, they demonstrate the diverse ways that people have adapted to a physical environment. For example, people around the world learned to make shelters out of available resources, whether 3.1: INTRODUCTION TO CULTURE 133 it was snow or mud bricks or wood. However, people used similar resources such as wood differently. In Scandinavia, people used trees to build cabins. In the American Midwest, people processed trees into boards, built a frame, and attached the boards to it. Many traits of folk culture continue today. Corn was first grown in Mexico around 10,000 years ago, and it is still grown there today. While many elements of folk culture exist side by side with modern culture, there are people whose societies have changed little, if at all, from long ago. These people practice traditional cultures, those which have not been affected by modern technology or influences. They often live in remote regions, such as some small tribes in the Amazon rainforest, and have scant knowledge of the outside world. As the lines continue blurring between cultural designations, the Amish of Pennsylvania are often referenced as both folk and traditional culture. Indigenous Culture When members of an ethnic group reside in their ancestral lands, and typically possess unique cultural traits, such as speaking their own exclusive language, they are considered an indigenous culture. Some indigenous peoples have been displaced from their native lands, but still practice their indigenous culture. Native Americans in the United States, such as the Navajo, have kept indigenous cultural practices. First Nations of Canada, such as the Inuit, have also retained their indigenous culture. Globalization and Popular Culture As a result of the Industrial Revolution, improvements in transportation and communication have shortened the time required for movement, trade, or other forms of interaction between two places. This development, known as space-time compression (see Topics 1.4 and 3.6), has accelerated culture change around the world. In 1817, a freight shipment from Cincinnati needed 52 days to reach New York City. By 1850, because of canals and railroads, it took half that long. And by 1852, it took only 7 days. Today, an airplane flight takes only a few hours, and digital information takes seconds or less. Similar change has occurred on the global scale. People travel freely across the world in a matter of hours, and communication has advanced to a point where people share information instantaneously across the globe. The increased global interaction has had a profound impact on cultures, from spreading English across the world to instant sharing of news, events and music. Globalization specifically refers to the increased integration of the world economy since the 1970s. The process of intensified interaction among peoples, governments, and companies of different countries around the globe has had profound impacts on culture. The culture of the United States is intertwined with globalization. Through the influence of its corporations, Hollywood movies, and government, the United States exerts widespread influence in other countries. But other countries also shape American culture. For example, in 2019, the National Basketball Association included players from 38 countries or territories. When cultural traits- such as clothing, music, movies, and types of 134 HUMAN GEOGRAPHY: AP. EDITION businesses-spread quickly over a large area and are adopted by various groups, they become part of popular culture. Elements of popular culture often begin in urban areas and diffuse quickly through globalization processes such as the media and Internet. These elements can quickly be adopted worldwide, making them part of global culture. People around the world follow European soccer, Indian Bollywood movies, and Japanese animation known as anime. With people in many nations wearing similar clothes, listening to similar music, and eating similar food, popular cultural traits often promote uniformity in beliefs, values, and the cultural landscape across many places The cultural landscape, also known as the built environment (see Topic 3.2), is the modification of the environment by a group and is a visible reflection of that group's cultural beliefs and values. Traditional Culture to Popular Culture Popular culture emphasizes trying what is new rather than preserving what is traditional. Many people, especially older generations or those who follow a folk culture, openly resist the adoption of popular cultural traits. They do this by preserving traditional languages, religions, values, and foods. While older generations often resist the adoption of popular culture, they seldom are successful in keeping their traditional cultures from changing, especially among the young people of their society. One clash between popular and traditional culture is occurring in Brazil. As the population expands to the interior of the rain forest, many indigenous cultures, like the Yanamamo tribe, have more contact with outside groups. Remaining isolated by the forest is becoming increasingly difficult as many young people from the indigenous cultures become exposed to popular culture and begin to integrate into the larger Brazilian society. As the young people leave their communities, they are more likely to accept popular culture at the expense of their indigenous cultural heritage, which threatens the very existence of their folk culture. Traditional culture typically exhibits horizontal diversity, meaning each traditional culture has its own customs and language that makes it distinct from other culture groups. Yet, people people within each group are usually homogeneous, or very similar to each other. By contrast, popular culture typically exhibits vertical diversity, meaning that modern urban societies are usually heterogeneous, or exhibiting differences, within the society and usually contain numerous multiethnic neighborhoods. However, on a global scale popular cultures are relatively similar with the same type of malls, shops, fast food, and clothing. Urban global culture centers are not identical, yet, global cities often do not have as much horizontal diversity across space as folk cultures. 3.1: INTRODUCTION TO CULTURE 135 COMPARING TRADITIONAL AND POPULAR CULTURE Trait Traditional Culture Popular or Global Culture Society • Rural and isolated location • Urban and connected location • Homogeneous and • Diverse and multiethnic indigenous population population • Most people speak an • Many people speak a global indigenous or ethnic local language such as English or language Arabic • Horizontal diversity • Vertical diversity Social • Emphasis on community and • Emphasis on individualism and Structure conformity making choices • Families live close to each • Dispersed families other • Weakly defined gender roles • Well-defined gender roles Diffusion • Relatively slow and limited • Relatively rapid and extensive • Primarily through relocation • Often hierarchical • Oral traditions and stories • Social media and mass media Buildings and • Materials produced locally, • Materials produced in distant Housing such as stone or grass factories, such as steel or glass • Built by community or owner • Built by a business • Similar style for community • Variety of architectural styles • Different between cultures • Similar between cities • Traditional architecture • Postmodern / contemporary architecture Food • Locally produced • Often imported • Choices limited by tradition • Wide range of choice • Prepared by the family or • Purchased in restaurants community Spatial Focus • Local and regional • National and global Artifacts, Mentifacts, and Sociofacts Whether a cultural attribute is considered traditional, folk, indigenous, or popular in nature, it is valuable to differentiate between elements of culture that can be seen and those that can not. There are artifacts that comprise the material culture, which consists of tangible things, or those that can be experienced by the senses. Art, clothing, food, music, sports, and housing types are all tangible elements of culture. Another element of the study of artifacts is understanding the techniques to use or build a specific artifact. Artifacts can be unique to a particular culture, or can be shared. For example, people of all cultures need to communicate through language, yet there are many groups that possess languages unique to their culture. The ability to read, write and understand the English language is an artifact of importance for much of popular global culture. 136 HUMAN GEOGRAPHY: AP" EDITION Mentifacts comprise a group's nonmaterial culture and consist ofintangible concepts, or those not having a physical presence. Beliefs, values, practices, and aesthetics (pleasing in appearance) determine what a cultural group views as acceptable and desirable. Mentifacts can also be unique or shared. People of many cultures possess an belief in one or many deities, and often the deities are unique to that culture. The belief in a god is a mentifact-the religious building or symbols are artifacts. Cultural groups also possess sociofacts, which are the ways people organize their society and relate to one another. Taken altogether, people tend to see the whole of their culture as greater than the sum of its individual parts. Sociofacts are embodied through families, governments, sports teams, religious organizations, education systems, and other social constructs. As with artifacts and mentifacts, sociofacts may also be unique or similar to other societies. Families are the foundations of most societies, yet what constitutes the structure of a family may vary widely between cultural groups. For example, Western cultures tend to view the nuclear family, consisting of the parents and their children as the basic family unit. By contrast, in many Western African cultures the norm is the extended family, consisting of several generations and other family members such as cousins living under one roof.Integrated Chinese Lesson 4Integrated ScienceIntegrated Chinese Lesson 5