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. Author manuscript; available in PMC: 2023 Aug 7.
Published in final edited form as: Pediatr Res. 2023 Feb 7;94(2):781–788. doi: 10.1038/s41390-023-02503-7

Influence of Puberty on Relationships Between Body Composition and Blood Pressure: A Cross-Sectional Study

Esther A Kwarteng 1, Lisa M Shank 2,3,4, Loie M Faulkner 1, Lucy K Loch 1, Syeda Fatima 1, Suryaa Gupta 1, Hannah E Haynes 1,2,4, Kaitlin L Ballenger 1, Megan N Parker 1,2, Sheila M Brady 1, Anna Zenno 1, Marian Tanofsky-Kraff 1,2,3, Jack A Yanovski 1,*
PMCID: PMC10403383  NIHMSID: NIHMS1868968  PMID: 36750741

Abstract

Background:

Fat mass (FM) and fat-free mass (FFM) are positively associated with blood pressure (BP) in youth. Yet, how puberty, independent of age, affects these relationships remains unclear. Given puberty may be a crucial period for cardiometabolic health, we examined how pubertal development moderates the associations of FM/FFM with BP.

Methods:

Pubertal development, resting BP, and body composition were assessed in a convenience sample of youth (5.5-17y). General linear models were conducted to assess if pubertal development moderated the relationships between FM/FFM and systolic/diastolic BP standardized for age, sex, and height (SBPz/DBPz).

Results:

Among participants (N=1,405; age: M=13.3±2.9y; 65.4% female; 53.2% racial/ethnic minority), FM/FFM were positively associated with SBPz and DBPz (ps≤.02). Pubertal development moderated the associations between FFM and BPz (ps≤.01), but not FM (ps>.43). For early/mid and late pubertal participants, there were positive associations between FFM and BP (DBPz: βs=.10-.18, ps≤.01; SBPz: βs=.33-.43, ps<.001); however, these relationships were attenuated, especially for prepubertal DBPz (DBPz: β=.01, p=.91; SBPz: β=.24, p=.001).

Conclusions:

Puberty moderated the relationships between FFM and SBPz/DBPz in analyses that separately modeled the contributions of age and sex. These data suggest that the FFM-DBPz association may potentially be impacted by increasing sex hormone concentrations during puberty.

Introduction

Puberty is a pivotal stage in life characterized by the morphological and physiological changes that occur as children transition into adulthood.1 Puberty generally begins between ages 8-14 years and has a duration of approximately 3-6 years;2 its onset is affected by genetic, neuroendocrine, and environmental factors including nutrition.3 During pubertal development, youth experience significant physical changes, especially in regard to secondary sexual characteristics, stature, and body structure. Breast development is typically the first indication of puberty in girls, which is primarily induced by ovarian estrogen secretion in response to increased pituitary gland gonadotropin secretion. In boys, testicular enlargement is the initial manifestation of puberty, which is the direct result of gonadotropin secretion.4

In addition to the development of these secondary sexual characteristics, drastic changes in body composition occur during puberty. As youth progress through puberty, height and weight increase.2 In early puberty, fat-free mass (FFM), the sum total of the body’s water, proteins, glycogen, and minerals,5 begins to increase in both sexes.6 In girls, FFM reaches its peak at menarche and then stabilizes, whereas in boys, FFM continues to rapidly increase throughout puberty.4 Conversely, the pattern in which fat mass (FM), primarily nonessential body lipids,5 accumulates in boys and girls during puberty is distinct from that for FFM. Over the course of puberty, girls typically gain FM while boys experience a significant FM reduction.7 The precise underlying mechanisms driving these physiological changes are not fully established, though it is likely they are at least in part related to differences in the hormonal milieux of male and female adolescents.7,8

Furthermore, blood pressure (BP) – generally measured as systolic blood pressure (SBP) and diastolic blood pressure (DBP) – tends to increase during maturation. By definition, SBP is the peak pressure of the arteries, and is measured as the onset of the “tapping” Korotkoff sounds.9-11 DBP is the arterial pressure at its lowest point, and is measured as the disappearance of the Korotkoff sounds.9-11 Studies have found that during prepuberty, girls have higher BP than boys.12,13 However, unlike the relatively steady increases by age and height found for both SBP and DBP,11,14 there have been inconsistent findings about changes in BP over the course of puberty in girls and boys. In one study, both boys and girls experienced pronounced BP increases during early/mid stages of puberty.15 Conversely, another found that BP was not higher in children and adolescents in late puberty than youth in earlier developmental stages.16 A third study found significant changes in the rate of increase in SBP and DBP, which occurred at different ages and pubertal statuses in boys and girls. From ages 10 to 13, the average BP of girls was higher than that of boys; however, mean SBP increased in boys during early/mid puberty and became higher than SBP in girls after approximately age 13.12 Though not fully consistent, these findings suggest that puberty may be associated with significant sex-differentiated BP changes.

Many studies have found positive associations between BP and height, weight, and body mass index (BMI, kg/m2) in youth.16-19 However, it is less clear how the association between body composition (FM/FFM) and BP varies across childhood development. One small cross-sectional study conducted in Italy13 found that BMI and lean mass were positively associated with SBP in both boys and girls who were prepubertal or in puberty, but these factors were positively associated with DBP in prepubertal and pubertal girls only. In addition, FM was positively associated with SBP for prepubertal and pubertal boys but not girls.13 A similar study found that FM was positively associated with SBP in both prepubertal and pubertal youth, but FM was not a significant predictor of DBP.20 In contrast, a cross-sectional South African study found both FM and FFM to be positively associated with BP in prepubertal and pubertal youth.21 A larger cross-sectional study conducted in Canada found that FM and FFM were positively associated with BP in pubertal boys and girls.22 An additional study found that the association between lean mass and BP strongly increased during pubertal growth in boys; this increase in association strength was not observed in girls.23 As such, there is preliminary evidence across studies to suggest that body composition may potentially impact BP differentially over the course of pubertal development.13,18,19 However, no study has directly examined if the associations between body composition and BP in youth are moderated by puberty independent of age.

Notably, childhood BP predicts BP in adulthood.24,25 Given that high BP in childhood and in adulthood are major risk factors for the development of adverse cardiovascular outcomes,25-28 it is important to understand predictors of childhood BP. We examined whether puberty moderated the relationships between BP and both FM and FFM in youth. As an exploratory aim, we also examined whether there was a three-way interaction between sex, puberty, and body composition on BP in youth.

Methods

Participants

We gathered a convenience sample from ten National Institutes of Health (NIH) research protocols (Supplemental Tables S1 and S2) that enrolled children (5.5-17 years old) between March 1996 and March 2020. Five protocols involved interventions targeting obesity (ClinicalTrials.gov IDs: NCT00005669; NCT00263536; NCT00680979; NCT01425905; NCT00001723), while the remaining five were non-intervention studies (ClinicalTrials.gov IDs: NCT00320177; NCT02390765; NCT00631644; NCT00001195; NCT00001522). Participants were recruited through mailings to families in the Washington, D.C. metropolitan area, physician referrals, newspaper advertisements, and flyers posted at local public facilities and distributed through local primary and secondary schools.

Across all obesity-intervention studies, youth were deemed eligible if they were at least 6 years of age and had a BMI ≥ 75th percentile for age and sex according to the Center for Disease Control and Prevention 2000 U.S. standards.29 Protocol-specific inclusion criteria are described in Supplemental Tables S1 and S2 and included hyperinsulinemia (ClinicalTrials.gov ID: NCT00005669), a history of or current episodes of loss-of-control eating (ClinicalTrials.gov IDs: NCT00263536; NCT00680979), prediabetes (ClinicalTrials.gov ID: NCT01425905), and an obesity-related comorbidity, such as Type 2 diabetes (ClinicalTrials.gov ID: NCT00001723). In all non-intervention protocols, inclusion criteria included: minimum age of 2 years, BMI ≥ 5th percentile for age and sex,29 and good general health. However, for the age minimum of this research, participants below 5.5 years were excluded in analyses due to the paucity of subjects aged 2-5.4 years.

Across all research protocols (intervention and non-intervention), children were excluded based on identification or history of major cardiovascular disease, medical illness, or any other serious obesity-related comorbidity, such as gall bladder disease; psychiatric condition; medication prescription that may affect weight, mood, and eating behaviors; and current pregnancy or history of pregnancy. No additional eligibility criteria were applied for analyses. All protocols were approved by the Institutional Review Board of the NIH.

Procedure

Prior to study participation, written informed consent and assent were obtained from parents and/or guardians and youth, respectively. All participants were seen at the Hatfield Clinical Research Center, NIH, in Bethesda, Maryland. For children and adolescents participating in intervention protocols, the data utilized were collected at baseline, prior to the initiation of treatment.

Measures

Demographics.

Reporting race and ethnicity in these research studies was mandated by the NIH, which is consistent with the Inclusion of Women, Minorities, and Children policy. Parents/guardians reported child race and ethnicity. The race of child participants was categorized as: Asian, Black or African American, Native American, Pacific Islander, White, or multiracial. The ethnicity of child participants was categorized as: Hispanic or Latino or not Hispanic or Latino. The child’s sex (male or female) was also collected based on parent/guardian report.

Anthropometric Measures.

Body weight was measured to the nearest 0.1 kilogram using a calibrated scale. Height was measured in triplicate to the nearest 0.1 centimeter using a digital stadiometer and used to calculate BMI (kg/m2). BMIz was calculated for sex and age in accordance with the Center of Disease Control growth standards.29

Body Composition.

Depending on the study protocol, FM and FFM were assessed with dual-energy x-ray absorptiometry (DXA; Hologic QDR2000 or QDR4500, Bedford, MA; or iDXA system; GE Healthcare, Madison, WI) or air displacement plethysmography (Bod Pod; Life Measurement Inc., Concord, CA). For DXA, lean mass and bone mineral content values were added together to calculate FFM. Both methods are validated measures of body composition in youth30-32 and have been successfully combined in previous studies.e.g.,33 Prior to the analysis of DXA and Bod Pod data, adjustments were made to enhance equivalence and comparability across sex and between body composition instrument measurements.34

Physical Examination.

Medical history and vital signs, obtained while seated and at rest, were assessed by a certified medical provider. SBP/DBP were obtained using an automated sphygmomanometer, with most measurements obtained using a Philips SureSigns VS3 (Cambridge, MA) or Dynamap (GE Heathcare, Piscataway, NJ) machine after selection of an appropriate cuff size for arm circumference. Blood pressure measurements were then standardized for age, sex, and height according to the computational approach of the U.S. National Heart, Lung, and Blood Institute (SBPz and DBPz).34 To determine pubertal stage, development was assessed through palpation to determine testicle size in males and inspection/palpation to determine breast Tanner stage in females.35-38 Boys with testes ≤3 mL and girls with Tanner Stage I breast development were considered to be prepubertal; boys with testes >3 mL to 15 mL and girls with Tanner Stages II and III breast development were considered to be in early/mid puberty, and boys with testes >15 mL and girls with Tanner Stages IV and V breast development were considered to be in late puberty.39

Statistical Analyses

All analyses were conducted using IBM SPSS Statistics 27 or 28. Data aggregated from all protocols were screened for normality and outliers. Seventy total participant data outliers (between 2-11 values for FM, FFM, SBP, SBPz, DBP, DBPz, height, heightz, BMI, and BMIz) were recoded to fit within three standard deviations from the mean,40 which resulted in normal distributions across all variables. Pearson correlations were conducted to examine the unadjusted relationships between body composition and BP. Four general linear models (GLMs) were also conducted to assess whether pubertal stage moderated the relationship between FM/FFM (expressed in kg) and SBP/DBP standardized for age, sex, and height (SBPz/DBPz).34 For each GLM, FM or FFM was the independent variable, SBPz or DBPz was the dependent variable, and categorical pubertal stage (prepuberty, early/mid puberty, late puberty) served as the moderator. Age and sex (coded as 0 = male and 1 = female) were included as covariates in all models. GLMs without age as a covariate were also conducted since SBPz and DBPz may already adjust for age; however, the direction and significance of puberty in these models were similar to those found with age included. Because of the long period of data collection, we also examined if the decade during which data were collected affected the analysis. We found the results of analyses for the key variables of interest were not changed in direction or significance. Therefore, results without decade modeled are shown in the manuscript. Similarly, adjusting for study type (treatment-seeking vs. non-treatment-seeking status) was considered as an additional covariate; however, its inclusion did not impact the significance or direction of any result. Thus, it was not included in the final models. For models with a significant moderation term, post-hoc GLMs were then utilized to examine the relationships between body composition and BP between each set of pubertal stages (prepuberty vs. early/mid; prepuberty vs. late; early/mid vs. late). If the moderation was significant for any combination of stages, within-group linear regression models were conducted to understand the relationship between body composition and BP within each pubertal stage. For the exploratory aim, we re-conducted the four GLMs, including all possible two-way interactions and the three-way interaction term between sex, body composition (FM or FFM), and pubertal stage. If the three-way interaction was significant for the combination of independent variables—sex, body composition, and pubertal stage—with blood pressure (SBPz or DBPz), a post-hoc GLM was conducted to understand whether pubertal stage moderated the relationship between body composition for BP within each sex. If the post-hoc two-way interaction was significant within boys or girls, within-group linear regression models were then conducted within the respective sex group to understand the relationship between body composition and BP within each pubertal stage.

Results

Participant Characteristics

A total of 1,405 participants (mean±SD age 13.3±2.9 years; BMIz=1.3±1.1; 65.4% female; 53.2% racial and ethnic minority individuals) were studied. Of the total sample of children and adolescents, 17.2% (n=242) were prepubertal, 28.8% (n=404) were in early/mid puberty, and 54.0% (n=759) were in the late pubertal group. Participant characteristics, overall and by sex and pubertal stage, are shown in Table 1. As expected, age, height, FM, FFM, SBP and DBP all increased across puberty for both girls and boys in the study (Table 1).

Table 1.

Participant Characteristics

Total
Sample
(N=1,405)		 Prepubertal
Boys
(n = 137)		 Prepubertal
Girls
(n = 105)		 Early/Mid
Pubertal
Boys
(n = 192)		 Early/Mid
Pubertal
Girls
(n = 212)		 Late
Pubertal
Boys
(n = 157)		 Late
Pubertal
Girls
(n = 602)		 p
Age (years), M±SD 13.3±2.9 9.7±2.3a 9.3±2.Da,b 12.7±2.1c 11.6±2.2d 15.6±1.4e 15.0±1.6f <.001
Race and Ethnicity, n(%) .04
Asian 63 (4.5%) 3 (2.2%)a 7 (6.7%)a,b 10 (5.2%)a,b,c 8 (3.8%)a,b,c,d 8 (5.1%)a,b,c,d,e 27 (4.5%)b,c,d,f
Black 527 (37.5%) 45 (32.8%)a 38 (36.2%)a,b 72 (37.5%)a,b,c 76 (35.8%)a,b,c,d 42 (26.8%)a,b,c,d,e 254 (42.2%)b,c,d,f
Hispanic/Latinx 83 (5.9%) 6 (4.4%)a 4 (3.8%)a,b 8 (4.2%)a,b,c 14 (6.6%)a,b,c,d 13 (8.3%)a,b,c,d,e 38 (6.3%)b,c,d,f
Multiracial 55 (3.9%) 4 (2.9%)a 5 (4.8%)a,b 8 (4.2%)a,b,c 7 (3.3%)a,b,c,d 5 (3.2%)a,b,c,d,e 26 (4.3%)b,c,d,f
Other or Unknown 19 (1.4%) 3 (2.2%)a 1 (1.0%)a,b 2 (1.0%)a,b,c 7 (3.3%)a,b,c,d 1 (0.6%)a,b,c,d,e 5 (0.8%)b,c,d,f
White, non-Hispanic 658 (46.8%) 76 (55.5%)a 50 (47.6%)a,b 92 (47.9%)a,b,c 100 (47.2%)a,b,c,d 88 (56.1%)a,b,c,d,e 252 (41.9%)b,c,d,f
Height (cm), M±SD 157.9±14.0 139.9±12.6a 137.6±12.0a,b 158.5±12.0c 152.3±10.6d 174.4±7.8e 163.1±6.7d <.001
Heightz, M±SD 0.5±1.1 0.4±1.2a 0.5±1.1aa,b 0.5±1.2a,b,c 0.7±1.2a,b,c,d 0.5±1.1a,b,c,d,e 0.4±1.0a,b,c,e,f .004
FM (kg), M±SD 26.0±15.7 20.5±13.5a 19.3±9.7a,b 25.6±18.5c 26.9±13.2c,d 18.3±16.0a,b,e 30.3±15.2f <.001
FFM (kg), M±SD 43.7±15.1 27.2±15.8a 27.1±11.4a,b 44.6±15.0c 37.4±12.9d 58.2±11.4e 48.6±9.8f <.001
BMI, M±SD 27.2±8.4 23.2±8.4a 22.8±6.7a,b 27.1±9.7c 26.6±7.5c,d 25.7±7.5a,c,d,e 29.4±8.1f <.001
BMIz, M±SD 1.3±1.1 1.1±1.2a 1.2±1.3a,b 1.3±1.3a,b,c 1.6±1.0c,d 0.9±1.1a,b,e 1.5±1.0b,c,d,f <.001
SBP (mmHg), M±SD 115.0±12.1 108.8±12.0a 110.4±12.3a,b 116.1±12.6c 113.2±12.5b,c,d 121.7±11.8e 115.8±10.8c,d,f <.001
SBPz, M±SD 0.6±1.1 0.5±1.1a 0.8±1.2aa,b 0.6±1.1a,b,c 0.7±1.2a,b,c,d 0.5±1.1a,b,c,d,e 0.5±1.0a,c,d,e,f .03
DBP (mmHg), M±SD 64.6±7.7 61.9±7.1a 63.2±7.4a,b 65.0±8.1b,c 64.3±7.7b,c,d 65.8±8.0b,c,d,e 65.2±7.5b,c,d,e,f <.001
DBPz, M±SD 0.04±0.7 0.1±0.6a 0.2±0.7a,b 0.1±0.7a,b,c 0.1±0.7a,b,c,d −0.04±0.7a,c,d,e −0.04±0.7a,e,f <.001
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Note. Tukey HSD test and Fisher’s exact tests were used to examine differences across groups. Different superscripts indicate statistically different groups, p<.05.

Abbreviations: FM = fat mass; FFM = fat-free mass; SBP = systolic blood pressure; DBP = diastolic blood pressure; kg = kilograms; mmHg = millimeters of mercury.

Fat Mass and Blood Pressure

Among the entire cohort, models revealed a positive relationship between FM and BPz (ps<.001; Figures 1A, 1B; Table 2). Pubertal stage did not significantly moderate the relationship between FM and SBPz (p=.60; Table 2A), or the relationship between FM and DBPz (p=.43; Table 2B). In exploratory modeling, the three-way interaction between sex, pubertal stage, and FM was not significant for SBPz (p=.34). However, there was a significant three-way interaction found for DBPz (p=.04). See full statistics for these exploratory models in Supplemental Tables S3A and S3B for SBPz and DBPz, respectively. In post-hoc GLM analysis for DBPz within each sex, there was no significant interaction between pubertal stage and FM in boys [F(2, 479)=1.74, p=.18] or girls [F(2, 911)=2.19, p=.11]. See Supplemental Tables S4A and S4B.

Figure 1. Associations between Body Composition and Standardized Systolic and Diastolic Blood Pressure.

Figure 1.

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After adjusting for sex and age, both fat mass (A) and fat-free mass (C) were significantly associated with systolic blood pressure standardized for age, height, and sex (SBPz). Similarly, both fat mass (B) and fat-free mass (D) were significantly associated with diastolic blood pressure standardized for age, height, and sex (DBPz).

Table 2.

General Linear Model Examining Fat Mass and Standardized Systolic (A) and Diastolic (B) Blood Pressure

Variable df F β η2p p
A. Systolic Blood Pressure
Corrected Model 7 32.90 -- .14 <.001
  Intercept 1 20.76 .93 .02 <.001
  Sex 1 3.55 −.12 .003 .06
  Age (y) 1 22.41 −.07 .02 <.001
  Fat Mass (kg) 1 124.14 .02 .08 <.001
  Pubertal Stage 2 .59 -- .001 .55
  Pubertal Stage*Fat Mass 2 .51 -- .001 .60
B. Diastolic Blood Pressure
Corrected Model 7 10.17 -- .05 <.001
  Intercept 1 3.65 .16 .003 .06
  Sex 1 .77 −.04 .001 .38
  Age (y) 1 7.11 −.03 .01 .01
  Fat Mass (kg) 1 18.36 .01 .013 <.001
  Pubertal Stage 2 1.46 -- .002 .23
  Pubertal Stage*Fat-Free Mass 2 .84 -- .001 .43
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Fat-Free Mass and Blood Pressure

Similar to FM, among the entire cohort, there was a positive association between FFM and BPz (ps≤.02; Figures 1C, 1D; Table 3). In addition, pubertal stage significantly moderated the relationship between FFM and SBPz (p=.002; Table 3A). Post-hoc analyses indicated that the relationship between FFM and SBPz differed between prepubertal youth and participants in the early/mid pubertal stage (p=.003), as well as prepubertal youth and participants in the late pubertal stage (p<.001), However, no significant difference was found between early/mid and late pubertal stage groups (p=.78). Within-group regression models indicated a significant positive association between FFM and SBPz in participants within all pubertal stage groups: prepubertal (β=.24, p=.001), early/mid pubertal (β=.43, p<.001), and late pubertal (β=.33, p<.001; Figure 2A). In our exploratory model, there was no significant three-way interaction between sex, pubertal stage, and FFM for SBPz (p=.81), See full statistics of this exploratory model in Supplemental Table S5A for SBPz.

Table 3.

General Linear Model Examining Fat-Free Mass and Standardized Systolic (A) and Diastolic (B) Blood Pressure

Variable df F β η2p p
A. Systolic Blood Pressure
  Corrected Model 7 23.77 -- .11 <.001
  Intercept 1 20.53 .57 .02 <0001
  Sex 1 9.40 .20 .01 .002
  Age (y) 1 57.43 −.13 .04 <.001
  Fat-Free Mass (kg) 1 99.58 .03 .07 <.001
  Pubertal Stage 2 6.76 -- .01 .001
  Pubertal Stage*Fat-Free Mass 2 6.31 -- .01 .002
B. Diastolic Blood Pressure
  Corrected Model 7 7.16 -- .04 <.001
  Intercept 1 3.59 .05 .003 <.001
  Sex 1 1.63 .05 .001 .20
  Age 1 9.73 −.03 .01 .002
  Fat-Free Mass 1 5.94 .01 .004 .02
  Pubertal Stage 2 4.97 -- .01 .01
  Pubertal Stage*Fat-Free Mass 2 4.83 -- .01 .01
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Figure 2. Relationship Between Fat-Free Mass and Standardized Systolic and Diastolic Blood Pressure Model within Each Pubertal Stage.

Figure 2.

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(A) After adjusting for age and sex, pubertal stage significantly moderated the relationship between fat-free mass and standardized systolic blood pressure (SBPz; p=.002). Post-hoc linear regression models within each pubertal stage indicated a positive association between fat-free mass and SBPz in all groups: prepuberty (β=.24, p=.001), early/mid (β=.43, p<.001) and late pubertal participants (β=.33, p<.001). (B) After adjusting for age and sex, pubertal stage significantly moderated the relationship between fat-free mass stage and standardized diastolic blood pressure (DBPz; p=.01). Post-hoc linear regression models within each pubertal stage indicated a positive association between fat-free mass and DBPz in early/mid (β=.18, p=.003) and late pubertal participants (β=.10, p=.01); this significance was not found in prepubertal youth (β=.01, p=.91).

Pubertal stage also moderated the relationship between FFM and DBPz (p=.01; Table 3B). Post-hoc analyses indicated that the relationship between FFM and DBPz was significantly different between the prepubertal and early/mid pubertal stage groups (p=.004), as well as the prepubertal and late pubertal stage groups (p=.004). However, no significant difference was found between early/mid and late pubertal stage groups (p=.89). Within-group regression models indicated a significant positive association between FFM and DBPz in participants within the early/mid pubertal (β=.18, p=.003) and late pubertal (β=.10, p=.01) stage groups. There was no significant association between FFM and DBPz in participants within the prepubertal stage (β=.01, p=.91; Figure 2B). In an exploratory model, there was no significant three-way interaction between sex, pubertal stage, and FFM for DBPz (p=.84). See full statistics of this exploratory model in Supplemental Table S5B for DBPz.

Discussion

This study of 1,405 healthy youth confirmed prior reports that FM and FFM are positively associated with both SBPz and DBPz. Pubertal stage did not significantly moderate the relationships between FM and BPz; however, puberty significantly moderated the association between FFM and both SBPz and DBPz. There was a significant positive association between SBPz and FFM within all pubertal stage groups but with a significantly smaller slope for prepubertal children. For DBPz, there was a significant positive association with FFM for participants within the early/mid and late pubertal stages, but not for participants within the prepubertal stage.

Pubertal stage did not moderate the significant positive relationship between FM and SBPz or DBPz. This finding supports previous studies showing that adiposity is significantly correlated with BP in youth of all pubertal stages,18,21,41-52 and our findings suggest that puberty may not greatly impact that relationship. In addition, in exploratory analyses, we did not find a three-way interaction between sex, pubertal stage, and FM for SBPz, suggesting that puberty did not significantly impact these relationships for either sex. Few studies have directly examined sex differences within the interaction between body composition and puberty. One small previous study found a positive association between FM and SBP in boys of all pubertal stages analyzed, prepubertal and pubertal. However, they found no significant association in girls, regardless of pubertal stage, perhaps due to the small sample size.13 Taken together, there is little evidence that pubertal stage is a significant moderator of the relationship between FM and SBP.

Our exploratory models identified a significant three-way interaction with FM for DBPz. However, post-hoc tests revealed no significant interaction between pubertal stage and FM in boys or girls. We are not aware of prior studies that have examined whether sex impacts the relationship between FM and DBP in pubertal boys and girls. However, FM has been found to be positively associated with DBP within all pubertal stages.17,20,22,42,53 As with SBP, these findings imply that other factors beyond puberty may impact the relationship between FM and DBP.

Most interestingly, we found that puberty significantly moderated the relationship between FFM and BPz. Both older and more recent studies have shown that FFM is positively associated with BP in boys and girls across pubertal stages,17,21,22,45,48,54 though some find the relationship is attenuated especially for DBP.42 Similarly, we found a significant positive association between FFM and SBPz within all pubertal groups; however, the relationship was attenuated in the prepubertal group. When examining DBPz, we found a significant positive association between FFM and DBPz in early/mid and late pubertal participants only; this relationship was not significant in prepubertal youth. Puberty is associated with a range of physiological and cardiometabolic changes in youth,2,6,7 potentially explaining this observed relationship. One possible mechanism may be the cardiovascular and renal effects of growth hormone, such as its ability to increase glomerular filtration rate and renal plasma flow.55 At the onset of puberty, growth hormone secretion increases in response to elevated concentrations of sex steroids.56,57 Higher growth hormone may increase the apparent impact of FFM on BP, as normal increases in growth hormone during puberty result in decreased peripheral vascular resistance and expansion in blood volume, leading to increased cardiac output.58,59 This direct role in cardiac output, and thus BP, is also proportional to FFM in that growth hormone stimulates both muscle growth (primarily via insulin-like growth factor 1)60 and bone formation and maturation.2

Another possible explanation for the moderation of puberty on the relationship between FFM and BP is insulin secretion. Many studies have shown that during puberty, insulin sensitivity decreases,61-63 which ultimately results in a compensatory increase of insulin secretion.64 The additional insulin during puberty may impact the relationship observed as insulin is known to increase renal sodium absorption, activate the sympathetic nervous system, and alter transmembrane ion transport,65 which are all known to increase BP. Similarly, faster, more sporadic secretion of insulin may also affect FFM by stimulating uptake of glucose by muscle, thus promoting muscle growth.66,67 However, it is also important to note that the attenuation of the association observed between FFM and BP in prepubertal children may potentially have been due to the restricted range of FFM in the current sample.

Lastly, there was no significant three-way interaction between sex, pubertal stage, and FFM for BP. Given that previous research has shown significant relationships between FFM and BP across puberty among both boys and girls,17,22,54 there may not be notable sex differences in these relationships across puberty. Therefore, it is possible that the pubertal effects that occur in both sexes, such as significant increases and effects of growth hormone and insulin, may have the most clinically relevant impact on the relationship between FFM and BP. Future research should longitudinally examine potential mechanisms explaining the relationship between pubertal stage, body composition, and BP in both boys and girls across pubertal development.

Study strengths include the analysis of a large and diverse sample size of youths. All analyses were conducted using standardized blood pressure (BPz), rather than raw BP measurements. This is a relative strength because BP in youth is affected by growth and maturation.68 Similarly, analyses included FM as measured by DXA or Air Displacement Plethysmography, which minimized the known limitations of using BMI.69,70 While previous studies have primarily focused on the relationship between FM and BP,20,41,53,71,72 our focus on both FM and FFM allowed for the understanding of how the totality of non-fat body mass components are impacted by pubertal growth.

Limitations of the current study include its cross-sectional nature, preventing the examination of differences within participants across puberty. Similarly, our sample had relatively fewer participants in the prepubertal pool, in comparison to the number of participants in the early/mid and late pubertal groups, potentially limiting our ability to detect small effects. Lastly, the current study did not include other potentially important covariates, such as physical activity, diet, and socioeconomic status, which may significantly impact growth patterns and BP levels during this pivotal stage of development.73-76 Future research should examine the relationship between body composition and BP longitudinally over the course of pubertal development, while also exploring potential mechanisms and covariates, such as sex hormones and physical activity.

This study sought to examine the relationships between body composition and BP throughout puberty. We found that puberty did not moderate the relationship between FM and BP but did moderate the relationship between FFM and BP in youth. It is possible that the sex hormone-induced increases in growth hormone and insulin secretion that occur during puberty result in decreased peripheral vascular resistance and increased renal sodium reabsorption, respectively, ultimately altering the relationship between FFM and BP at the onset of puberty. Further elucidating the relationships among body composition and BP across development is essential to develop a solidified understanding of how puberty affects cardiometabolic health during childhood. Future research should attempt to replicate these findings in boys and girls using a longitudinal prospective study design throughout childhood.

Supplementary Material

1

IMPACT:

  • Fat mass (FM) and blood pressure (BP) were positively associated throughout puberty.

  • Fat-free mass (FFM) and BP were positively associated throughout puberty; however, puberty moderated the FFM-BP relationship, such that there was a positive relationship in early/mid and late puberty, but the relationship was attenuated for prepubertal children.

  • These findings contribute further insight into physiological and cardiometabolic changes occurring during puberty.

  • Changes in hormone concentrations may explain the impact puberty has on the FFM-BP relationship.

  • Understanding predictors of BP are important as childhood BP is associated with future cardiometabolic outcomes.

ACKNOWLEDGMENTS:

Special thanks to the study participants and their families for volunteering their time to participate in the research studies used for analyses.

FUNDING:

This work was supported by the Intramural Research Program of the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) Grant number ZIA-HD00641; J. Yanovski, with supplemental funding from the Division of Nutrition Research Coordination, the National Institute of Minority Health and Health Disparities, and the Office of Behavioral and Social Sciences Research (to JAY). Additional monetary support derived from the NICHD National Research Service Award 1F32HD056762; NICHD Grant K99-R00HD069516; Uniformed Services University of the Health Sciences Grant R072IC); National Institute of Kidney Diabetes and Digestive and Kidney Diseases Grant R01DK080906-04.

Footnotes

COMPETING INTERESTS: The authors declare no conflict of interest for this research. JAY reports unrelated grant funds to NICHD supporting his research from Soleno Therapeutics, Rhythm Pharmaceuticals, and Hikma Pharmaceuticals. The opinions and assertions expressed herein are those of the authors and are not to be construed as reflecting the views of the National Institutes of Health or the United States Department of Defense.

CONSENT STATEMENT: Prior to study procedures, written informed consent and assent were obtained from parents and/or guardians and youth, respectively.

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

1
NIHMS1868968-supplement-1.pdf (226.5KB, pdf)

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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