Other imaging techniques to quantify internal-abdominal adiposity (IA-AT) and subcutaneous-abdominal adiposity (SCA-AT) are frequently impractical in infants. The aim of this study was twofold: (a) to validate ultrasound (US) visceral and subcutaneous-abdominal depths in assessing IA-AT and SCA-AT from MRI as the reference method in infants and (b) to analyze the association between US abdominal adiposity and anthropometric measures at ages 3 months and 12 months. Twenty-two infants underwent MRI and US measures of abdominal adiposity. Abdominal US parameters and anthropometric variables were assessed in the Cambridge Baby Growth Study (CBGS),
Childhood obesity has become a major public health issue and its prevalence is increasing worldwide [
Several epidemiological studies have reported that early life factors, such as impaired fetal growth or excess postnatal weight gain, are associated with later obesity and related comorbidities [
Ultrasound (US) has been assessed as a noninvasive estimate of IA-AT and SCA-AT. US-visceral depth and US abdominal-subcutaneous depth have been shown to be reliable and reproducible estimates of IA-AT and SCA-AT, respectively, when compared to CT or MRI in adults and in adolescents [
The validation study was carried out in a convenience sample of 22 healthy term singleton newborn infants (10 boys and 12 girls). Mothers and babies were recruited from the Neonatal Unit and postnatal wards of the Chelsea and Westminster Hospital, London, UK, between 2008 and 2009 and attended the Robert steiner MRI Unit, Hammersmith Hospital, London, UK. This study was approved by the Hammersmith and Queen Charlotte’s & Chelsea Hospital research ethics committee. Written parental consent was obtained prior to the participants’ visit.
Details of the study have been described elsewhere [
Infants characteristics in the Cambridge Baby Growth Study with ultrasound measures at 3 months, 12 months and both at 3 and 12 months1.
US at 3 months only | US at 12 months only | US at 3 and 12 months | ||||
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Birth | ||||||
Gestational age at birth (weeks) |
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Weight (kg) |
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Length (cm) |
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Ponderal index (kg/m3) |
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Sum of skinfolds (cm) |
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1Data are means (±standard deviations).
US: ultrasound.
In the validation study, weight, length, and waist circumference (WC) were measured by one of three trained clinical research fellows. Weight was measured using a Marsden Professional Baby Scale (London, UK) and recorded to the nearest 0.1 kg. Crown-heel length was measured with a Rollameter, a recumbent infant board with a sliding footboard (Raven Equipment Ltd., Dunmow, Essex, UK). WC was measured at the midpoint between the inferior border of the costal margin and the anterior superior iliac crests using a D-loop tape measure (Chasmors Ltd., London, UK) [
In CBGS, infants were measured at birth, 3 months, and 12 months by trained paediatric nurses or research assistants. Weight was measured to the nearest 1 g using a SECA 757 digital scale (Chasmors Ltd.) and length using a Kiddimeter (Chasmors Ltd). WC was measured as described previously. Triceps, quadriceps, flank, and subscapular skinfold thicknesses were measured in triplicate on the left side of the body using Holtain calipers (Chasmors Ltd). The triceps skinfold was measured halfway between the acromial process and the olecranon. The quadriceps skinfold was taken from a vertical line over the quadriceps muscle at midline of the thigh, and half way between the top of the patella and the inguinal crease. The flank (posterior suprailiac) skinfold was taken from the diagonal plane in line with the natural angle of the iliac crest taken in the posterior axillary line immediately posterior to the iliac crest. The skinfold was taken at the oblique angle below the left scapula [
US-visceral depth and US-subcutaneous-abdominal depth were measured using a Logiq Book XP ultrasound, with a 3C MHZ -RS abdominal curved array transducer (both from GE Healthcare, Bedford, UK). For both measures, the transducer was positioned where the xiphoid line intercepted the WC measurement plane, and the images were taken during expiration. US-visceral depth was measured on a longitudinal plane with a probe depth of 9 cm and was defined as the distance between the peritoneal boundary and the corpus of the lumbar vertebra. US-subcutaneous abdominal depth was measured at the same location, but on a transverse plane with a probe depth of 4 cm, and was defined as the distance between the cutaneous boundary and the linea alba. The image was captured when the transducer just had contact with the skin to avoid compressing the subcutaneous adipose area. In the validation study, the US measures were performed by one of two trained operators and in CBGS by one of four trained operators. The relative intraobserver technical error of measurement (TEM) ranged between 0.3% and 1.7% for US-visceral depth, and 1.1% and 2.6% for US-subcutaneous-abdominal depth, and the relative interobserver TEM was 3.2% for US-visceral depth 3.6% for US-subcutaneous-abdominal depth, based on repeated measurements in 12 infants. In the validation study, qualitative information on the feasibility and acceptability of US was collected from the participants using open-ended questions.
The MRI procedure used in the validation study is described elsewhere [
Statistical analyses were performed using STATA version 11.0 (StataCorp Ltd.). Means and standard deviations are presented separately for boys and girls and sex differences were tested using unpaired
For CBGS, Pearson’s correlation coefficients were used to describe cross-sectional associations between US depths at 3 or 12 months and anthropometric variables. Associations between growth parameters at birth (birth weight and skinfolds SDS) and US depths at 3 or 12 months were tested using linear regression models. Associations were similar in both sexes, so all analyses were performed in the total sample with adjustment for sex. Further adjustment for current size (weight or skinfolds SDS) was included in the final models. Colinearity between parameters in the same model was quantified using the variance inflation factor (VIF); models with VIF > 5 were considered invalid [
All body composition variables and the residuals of the regression models were normally distributed. Statistical significance was set at
In the 22 newborn infants, mean range for age was 10.6 (6–19) days; gestational age at birth 39.9 (37.1–40.8) weeks; weight 3.3 (2.5–3.9) kg; length 53.1 (47–57) cm; WC 34 (29–39) cm; IA-AT 18 (8–32) cm3, SCA-AT 104 (59–202) cm3; US-visceral depth 2.0 (1.2–3.0) cm; and US-subcutaneous abdominal depth 0.30 (0.2–0.4) cm.
IA-AT showed moderate positive correlations with US-visceral depth (
Validation study: intercorrelations between MRI IA-AT or SCA-AT and anthropometry or ultrasound measures in 22 term infants.
IA-AT | SCA-AT | Total |
Ponderal Index | Length | Weight | US-SC-abdo depth | US-visceral depth | |
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(cm3)1 | (cm3)2 | (cm3)3 | (kg/m3) | (cm) | (kg) | (cm)4,5 | ||
SCA-AT (cm3)2 | 0.48* | 1 | ||||||
Total SC-AT (cm3)3 | 0.61* | 0.94** | 1 | |||||
Ponderal Index (kg/m3) | 0.15 | 0.32 | 0.27 | 1 | ||||
Length (cm) | 0.34 | 0.40* | 0.54* | −0.40* | 1 | |||
Weight (kg) | 0.39 | 0.6* | 0.70** | 0.2 | 0.81** | 1 | ||
US-SC-abdo depth (cm)4,5 | 0.52* | 0.71** | 0.78** | 0.17 | 0.79** | 0.92** | 1 | |
US-visceral depth (cm)3 | 0.48* | 0.22 | 0.31 | 0.14 | 0.31 | 0.40* | 0.38 | 1 |
Waist (cm) | 0.08 | 0.16 | 0.26 | 0.19 | 0.54* | 0.72** | 0.6* | 0.28 |
Values are Pearson’s correlation coefficients.
*
1IA-AT: internal-abdominal adipose tissue volume by MRI.
2SCA-AT: subcutaneous-abdominal adipose tissue volume by MRI.
3Total SC-AT: total body subcutaneous adipose tissue volume by MRI.
4US: Ultrasound.
5SC-abdo depth: subcutaneous-abdominal adipose tissue depth.
Prediction models for IA-AT and SCA-AT in the validation study.
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Model1 | Constant |
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RMSE7 |
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Weight |
Sex |
Age (days) |
US SC-abdo depth (cm)4,5 | US-visceral depth (cm)4 | ||||||
IA-AT (cm3)2 | 1 | −1.4 |
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— | — | — | — | 15 | 61.3 |
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2 | −1.5 |
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— | — | — | 16 | 59.8 |
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3 | −0.7 |
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−0.8 ± 3.2 |
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— | — | 22 | 60.0 |
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4 | 23.7 | −12.9 ± 8.0 | −0.3 ± 2.9 |
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— | 43 | 53.4 |
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5 | 20.9 | −15.0 ± 6.7 |
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62 | 37.4 |
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SCA-AT (cm3)3 | 1 | −42.6 |
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— | — | — | — | 36 | 38.2 |
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2 | −48.6 |
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— | — | — | 44 | 37.4 |
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3 | −49.4 |
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−0.3 ± 1.2 | — | — | 44 | 34.8 |
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4 | 66.7 | −47.4 ± 0.03 |
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— | 65 | 20.2 |
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1Covariables were added sequentially to the prediction models to demonstrate their incremental benefits.
2IA-AT: internal-abdominal adipose tissue volume by MRI.
3SCA-AT: Subcutaneous abdominal adipose tissue volume by MRI.
4US: Ultrasound.
5SC-abdo: subcutaneous-abdominal.
6
7RMSE: root mean square error.
8
Scatterplot of ultrasound visceral depth against MRI intra-abdominal adipose tissue (IAT-AT) mass. Correlation coefficient:
Scatterplot of ultrasound subcutaneous-abdominal depth against MRI subcutaneous-abdominal adipose tissue (SCAT-AT) mass. Correlation coefficient:
Eleven mothers provided qualitative comments regarding the measurements. Nine mothers commented favourably on the shorter duration of US compared to MRI, and four commented favourably on the lack of separation from their infants using US.
Characteristics of CBGS infants with US measures at age 3 months (
Summary of measurements in Cambridge Baby Growth Study infants.
Boys | Girls |
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Birth |
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Gestational age at birth (weeks) |
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Weight (kg) |
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Length (cm) |
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Ponderal index (kg/m3) |
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Sum of skinfolds (cm) |
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3 months2 |
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Weight (kg) |
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Length (cm) |
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Ponderal index (kg/m3) |
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Sum of skinfolds (cm) |
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US-visceral depth (cm) |
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US-subcut abdo depth (cm) |
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12 months3 |
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Weight (kg) |
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Length (cm) |
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Ponderal index (kg/m3) |
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Sum of skinfolds (cm) |
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US-visceral depth (cm)4 |
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US-subcut abdo depth (cm)4 |
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Data are means (±standard deviation).
1Student’s t-test was used to compare boys versus girls.
23-month ultrasound measurements were performed in 487 infants (254 boys and 233 girls).
312-month ultrasound measurements were performed in 495 infants (258 boys and 237 girls).
4US: ultrasound.
Mean US-visceral depth at age 12 months was 22% higher in boys and 17% higher in girls at 12 months than at 3 months. In contrast, mean US-subcutaneous abdominal depth and skinfold thickness did not change with age. The apparent increase in US-visceral depth was confirmed in the 360 infants with repeat measures at both 3 and 12 months (mean change: +0.4 cm;
In cross-sectional analyses (Table
Cross-sectional correlations between anthropometry1 and abdominal ultrasound measures at 3 months (487 infants) and 12 months (495 infants). Data are Pearson’s coefficients.
US-visceral depth | US-subcutaneous abdominal depth | |||
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3 months | 12 months | 3 months | 12 months | |
Anthropometry at 3 months | ||||
Weight SDS | 0.02 | 0.31** | ||
Length SDS | −0.05 | 0.20** | ||
Ponderal index SDS | 0.11* | 0.27** | ||
Mean of skinfolds SDS | 0.05 | 0.31** | ||
Anthropometry at 12 months | ||||
Weight SDS | 0.03 | 0.30** | ||
Length SDS | 0.00 | 0.11** | ||
Ponderal index SDS | 0.04 | 0.26** | ||
Mean of skinfolds SDS | 0.10* | 0.30** |
1SDS: sex- and age-adjusted standard deviation scores.
2US: ultrasound.
*
In models without adjustment for current body size, US-visceral depth at 3 months (
Associations between size at birth and ultrasound abdominal depth measurements at 3 months (487 infants) and 12 months (495 infants).
Birth weight SDS |
Mean skinfold thickness SDS at birth | |||
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Model 1 | ||||
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US-visceral depth (cm) | ||||
3 months | −0.024 ± 0.027 |
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−0.059 ± 0.031 |
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12 months | −0.041 ± 0.024 |
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US-subcut abdo depth (cm) | ||||
3 months | 0.005 ± 0.005 |
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12 months | 0.002 ± 0.004 |
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0.007 ± 0.005 |
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Model 2 | ||||
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US-visceral depth (cm) | ||||
3 months | −0.041 ± 0.031 |
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− |
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12 months | −0.045 ± 0.026 |
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− |
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US-subcut abdo depth (cm) | ||||
3 months | − |
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0.005 ± 0.005 |
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12 months | − |
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0.002 ± 0.005 |
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Results are shown before (Model 1) and after (Model 2) adjustment for body size at the time of the ultrasound measurement.
Model 1: adjusted for sex.
Model 2: also adjusted for current weight or skinfolds, respectively.
1
Our validation study results showed that US abdominal depth provides acceptable accuracy in estimating IA-AT and SCA-AT volumes assessed by MRI in infants. The US measures showed stronger correlations with IA-AT and SCA-AT than did the traditional anthropometric variables, and the addition of US measures to those variables substantially improved the predictions of IA-AT and SCA-AT. The precision of our models was significantly improved as RMSE for IA-AT and SCA-AT substantially decreased. Furthermore, the reproducibility and reliability of the US measures were high as indicated by low inter- and intraobserver technical errors of measurement. In addition, the ultrasound method was highly acceptable to parents as it was faster to perform than MRI and no separation from their infants was required. By contrast, the actual MRI scanning time is approximately 12 minutes, but the whole procedure including preparation time to settle the infant can take up to one hour.
We acknowledge that our validation study has some limitations. In particular, it was performed in newborns at age range 6–19 days, rather than at 3 or 12 months as in CBGS. This is because the reference imaging techniques, MRI and CT, are not feasible for research studies at those later ages, as discussed previously. However, our findings are consistent with positive reports in adults and adolescents comparing abdominal US to MRI [
Secondly, the sample size in our validation study was small (
Finally, the correlation between US-visceral depth and IA-AT was only moderate (
In the CBGS cohort study, we found that infants with lower skinfold thickness at birth tended to have
We also observed that the associations between skinfold thickness at birth and infancy visceral depth strengthened with further adjustment for current skinfold thickness. Some investigators have argued that adjustment for current size could potentially introduce bias due to overcontrolling [
Therefore, postnatal factors related to infancy gains in skinfold thickness may influence the accumulation of visceral adipose tissue at 3 and 12 months. Our observation of weak tracking in visceral depth indicates wide between-individuals variation in the rate of accumulation of visceral adipose tissue during infancy, although measurement error and imprecision are likely contributing factors to this estimate. Our observed associations with breastfeeding indicate that postnatal nutrition may influence the accumulation of visceral adipose tissue in infancy.
In conclusion, US abdominal depths were better than anthropometric measures in ranking infants with higher or lower IA-AT and SCA-AT volumes and may be applicable to large epidemiological studies at young ages when MRI and CT imaging techniques are infeasible. Application of these US measures in a large birth cohort study showed that visceral and subcutaneous-abdominal depths differed in their changes with age and in their patterns of association with antenatal and postnatal factors, suggesting that IA-AT and SCA-AT may be differentially regulated in the first year of life.
None of the authors had any conflict of interest.
The authors are grateful to all the families who participated in the London validation and Cambridge Baby Growth studies; the Cambridge Baby growth Study team (pediatric research nurses, research assistants, and data managers); the staff at the Addenbrooke’s Wellcome Trust Clinical Research Facility; and the midwives at the Rosie Maternity Hospital, Cambridge, UK. They also thank the Senior Research Radiographer, Giuliana Durighel, from the Robert Steiner MR Unit for her technical assistance and the Clinical Research Fellows (Dominika Betakova, Karen Logan, Rikke Ruager-Martin, and Anne Dolan) from Chelsea and Westminster’s Hospital, Imperial College, London, UK, for recruitment and support during data collection. The Cambridge Baby Growth Study was supported by the Medical Research Council (MRC), UK, the World Cancer Research Fund International, the European Union (EU Framework V), the Newlife Foundation, and the Cambridge Biomedical Research Centre.