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Obstetrics & Gynecology 1999;94:209-212
© 1999 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Subcutaneous Fat in the Fetal Abdomen as a Predictor of Growth Restriction

FRANÇOIS GARDEIL, MRCOG, RICHARD GREENE, MRCOG, BERNARD STUART, FRCOG and MICHAEL J. TURNER, FRCOG

From the Coombe Women’s Hospital, Dublin, Republic of Ireland.

Address reprint requests to: Francçois Gardeil, MRCOG Coombe Women’s Hospital Dublin 8, Republic of Ireland E-mail: gardeil{at}iol.ie


   Abstract
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Abstract
Material and Methods
 Results
 Discussion
 References
 
Objective: To determine if measuring fetal abdominal fat antenatally using ultrasound can predict fetal growth restriction (FGR).

Methods: One hundred thirty-seven unselected women with singleton pregnancies had serial ultrasound scans at 20, 26, 31, and 38 weeks’ gestation. Subcutaneous fat in the fetal abdomen was measured using the same section as the abdominal circumference (AC). Outcome measures were birth weight, neonatal morbidity, and ponderal index.

Results: Infants with subcutaneous fat less than 5 mm at 38 weeks (n = 51) were almost five times more likely to have a birth weight below the 10th centile than those with subcutaneous fat of 5 mm or more (n = 75). The incidence of neonatal morbidity was significantly higher in infants with subcutaneous fat less than 5 mm, compared with those with subcutaneous fat of 5 mm or more (20% versus 8%, P < .05). Decreased subcutaneous fat was also associated with a high prevalence of low ponderal index, regardless of birth weight category.

Conclusion: Measurement of fat in the abdominal wall is a simple technique with a sensitivity for predicting low birth weight similar to that of conventional sonography and might potentially predict FGR irrespective of fetal weight.

Fetal growth restriction (FGR) might be defined as the suppression of genetic growth potential that occurs in response to impaired nutrient oxygen supply to the fetus. It is a cause of perinatal death and is associated with significant neonatal morbidity. Adaptation to a limited supply of intrauterine nutrient might increase the risk of coronary heart disease, hypertension, and insulin resistance in later life.1,2

Severe FGR often results in births of infants who weigh less than the 10th centile for gestation. The majority of small infants, however, are well nourished. Evidence of FGR can be found in infants of apparently normal weight.3 The statistical classification of infants into weight centile categories4 has limited value in the assessment of fetal nutrition.

Antenatal diagnosis of FGR remains a challenge. Ultrasonography is the best technique, estimating fetal weight and growth velocity using multiple parameters. Body proportionality indices such as ratio of head-to-abdominal circumference5 and Doppler ultrasound studies6 can provide additional information. Diagnosis is easier at birth because growth-restricted infants show typical changes in body proportionality. Subcutaneous adipose tissue that acts as an energy source and insulator against hypothermia is reduced.7

Subcutaneous fat, which can be evaluated by means of skinfold thickness, can be seen antenatally with ultrasound. On a transverse section of the fetal abdomen, it appears as a well-delineated echogenic line and has been described previously by two investigators.8,9 We conducted a prospective study involving serial measurements of subcutaneous fat in the abdominal wall to determine whether it could predict FGR.


   Material and Methods
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Abstract
 Material and Methods
Results
 Discussion
 References
 
Beginning in November 1996, we invited all women presenting for their first antenatal visits at the Coombe Women’s Hospital to participate in our study by having serial ultrasound scans at 20, 26, 31, and 38 weeks’ gestation. However, enrollment was limited to 12 per week. The volunteers gave informed consent and had early sonographic confirmation of dates, and multiple pregnancies were excluded. Scans were done by two operators (FG and RG) with an Ultramark 4 Plus Ultrasound System (Advanced Technology Laboratories, Bothell, WA). Standard sections used for abdominal circumference (AC) were obtained, and subcutaneous fat in abdominal walls was measured in millimeters on the anterior abdominal wall, anterior to the margins of the ribs, using magnification (Figure 1Go). Biparietal diameter (BPD), occipitofrontal diameter, head circumference (HC), and AC and femur length (FL) were also measured routinely. With the exception of subcutaneous fat, all the sonographic findings were reported to clinicians caring for the women.



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  		Figure 1. Measurement of subcutaneous fat in the fetal abdomen.

 
By December 1997, 137 women had delivered. This study group was similar to the hospital population. All women but one were Irish. The mean age was 29 years. Forty-one percent of the women were nulliparous. We also selected 24 women (six at each gestation) to assess interobserver reproducibility. The two operators made the same measurements in 23 cases. Outcome measures were birth weight, weight-to-length ratio (ponderal index in kg/m3), and perinatal outcome. For birth weights we used our own hospital centiles.10 We defined two groups of infants at follow-up, those with subcutaneous fat thickness of less than 5 mm at 38 weeks and those with 5 mm or more. Between-group differences in rates of morbidity and incidence of low ponderal index were tested for significance by {chi}2 analysis. A statistical significance level of P < .05 was accepted.


   Results
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Abstract
 Material and Methods
 Results
Discussion
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Table 1Go shows the subcutaneous fat measurements made during the study. At 20 weeks’ gestation, the layer of subcutaneous fat could only be identified in 102 of 137 fetuses. Eleven women (8%) delivered before 38 weeks. The range and mean of subcutaneous fat measurements increased with gestation. Sixty-two women delivered between 38 and 40 weeks’ gestation. The remaining 64 women delivered between 40 and 42 weeks.


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  		Table 1. Measurements of Subcutaneous Fat
 
Table 2Go shows the birth weight centiles for gestational age using a cutoff point of 5 mm at 38 weeks’ gestation. Of the 51 infants with subcutaneous fat thickness of less than 5 mm, 16 (31.4%) weighed less than the 10th centile. Only 5 (6.7%) of 75 infants with measurements of 5 mm or more weighed less than the 10th centile. A subcutaneous fat thickness of less than 5 mm at 38 weeks had a sensitivity of 76.2% (16 of 21) and a specificity of 66.6% (70 of 105) for predicting birth weight below the 10th centile. Ultrasound estimation of fetal weight, based on standard biometry parameters at 38 weeks, had a sensitivity of 80.1% and a specificity of 96% for predicting birth weight below the 10th centile in this series. An infant with subcutaneous fat of less than 5 mm was almost five times more likely to have birth weight below the 10th centile than was an infant with subcutaneous fat of 5 mm or more. None of the 33 infants with subcutaneous fat of 6 mm or more had birth weights below the 10th centile.


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  		Table 2. Birth Weight Centiles According to Subcutaneous Fat Thickness at 38 Weeks
 
There were no perinatal deaths. Table 3Go shows neonatal morbidity. The incidence of neonatal morbidity was significantly higher in infants with subcutaneous fat of less than 5 mm (P < .05). There was no morbidity among the five infants who weighed less than the 10th centile who had subcutaneous fat thickness of 5 mm or more at 38 weeks.


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  		Table 3. Subcutaneous Fat Thickness at 38 Weeks and Neonatal Morbidity
 
We determined ponderal index, based on accurate crown–heal length measured at birth, for 99 of 126 infants delivered after 38 weeks. Of those 99 infants, 45 had subcutaneous fat of less than 5 mm at 38 weeks and 54, subcutaneous fat of 5 mm or more. The prevalence of low ponderal index (less than 24 kg/m3) was higher among infants with fat of less than 5 mm than those with 5 mm or more (20% versus 5%, P < .05).

Although the thickness of subcutaneous fat increased with gestation in the majority of cases, nine infants in our study had measurements lower at 38 than at 31 weeks’ gestation. Three of the nine, who all had subcutaneous fat less than 5 mm at 38 weeks, weighed below the 10th centile and had ponderal indices of less than 24 kg/m3. The other six infants had a birth weights within normal range. Four had ponderal indices calculated, which were less than 24 kg/m3 in three cases. The three infants with low ponderal indices and birth weights above the 10th centile had neonatal morbidity.


   Discussion
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Abstract
 Material and Methods
 Results
 Discussion
References
 
Assessment of fetal size and growth is important for antenatal care. It is hoped that early recognition of an abnormality, appropriate surveillance, and intervention will optimize perinatal outcomes. Although duration of labor and the need for operative delivery for dystocia increase with fetal weight,11 obstetricians concentrate on identifying small-for-gestational-age fetuses. The diagnostic value of conventional ultrasound for detecting small infants is established, with varying degrees of predictive ability quoted for different ultrasound parameters.12 Our study showed a thin layer of subcutaneous fat at 38 weeks’ gestation associated with low birth weight. Using a cutoff point of 5 mm, we could detect 76.2% of infants who weighed less than the 10th centile at birth. Although sensitivity of measurements compared favorably with conventional ultrasound biometry, specificity and predictive values were low. Measurement of subcutaneous fat in the fetal abdominal wall cannot replace sonographic estimation of fetal weight; however, it is a simple and fast technique that could be used as a screening test and might complement existing sonographic parameters.

Growth restriction, with its metabolic complications, can be found in infants of normal weight,3,13 and the majority of small infants are not growth restricted, so there is a need to evaluate characteristic that might predict nutrition status beyond birth weight. Protein–calorie deprivation results in soft-tissue wasting with relatively spared skeletal growth. The ponderal index,14 a weight-to-height ratio that shows this asymmetry, is a recommended outcome measure for studies on growth restriction.7 A low ponderal index in neonates is a major predictor of poor outcomes.15 Our results show that subcutaneous fat of less than 5 mm at 38 weeks’ gestation appears to associate with low ponderal index at birth. Our study showed that the incidence of neonatal morbidity was significantly higher in infants with a subcutaneous fat of less than 5 mm at 38 weeks, compared with infants with a subcutaneous fat of 5 mm or more. A decrease in subcutaneous fat thickness in the third trimester was also associated with a high incidence of low ponderal index and neonatal morbidity.

This study raises the exciting possibility that measurement of subcutaneous fat in the abdominal wall might help predict nutrition status antenatally, irrespective of weight. That could minimize unnecessary obstetric intervention for small, well-nourished fetuses and detect true FGR in infants of apparently normal weight, a high-risk group rarely identified with current methods of antenatal care. A larger study will be necessary to determine the independent predictive power of measurement of subcutaneous fat in the fetal abdomen.


   Footnotes
 
PII S0029-7844(99)00270-7

Received October 2, 1998. Received in revised form January 25, 1999. Accepted February 10, 1999.


   References
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Abstract
 Material and Methods
 Results
 Discussion
 References
 
1. Barker DJ. The long-term outcome of retarded fetal growth. Clin Obstet Gynecol 1997;40:853–63.[Medline]

2. Martyn CN, Barker DJ, Osmond C. Mothers’ pelvic size, fetal growth, and death from stroke and coronary heart disease in men in the UK. Lancet 1996;348:1264–8.[Medline]

3. Chard T, Costeloe K, Leaf A. Evidence of growth restriction in neonates of apparently normal weight. Eur J Obstet Gynaecol Reprod Biol 1992;45:59–62.[Medline]

4. Battaglia FC, Lubchenco LO. A practical classification of newborn infants by birth weight and gestational age. J Pediatr 1967;71:159–63.[Medline]

5. Campbell S, Thoms A. Ultrasound measurement of the fetal head to abdomen circumference ratio in the assessment of growth retardation. Br J Obstet Gynaecol 1977;84:165–74.[Medline]

6. Stuart B, Drumm J, Fitzgerald DE, Duignan NM. Fetal blood velocity waveforms in normal pregnancy. Br J Obstet Gynaecol 1980;87:780–5.[Medline]

7. Beattie RB, Johnson P. Practical assessment of neonatal nutrition status beyond birthweight: An imperative for the 1990s. Br J Obstet Gynaecol 1994;101:842–6.[Medline]

8. Hill LM, Guzick D, Boyles D, Merolillo C, Ballone A, Gmiter P. Subcutaneous tissue thickness cannot be used to distinguish abnormalities of fetal growth. Obstet Gynecol 1992;80:268–71.[Abstract/Free Full Text]

9. Petrikovsky BM, Oleschuk C, Lesser M, Gelertner N, Gross B. Prediction of fetal macrosomia using sonographically measured abdominal subcutaneous tissue thickness. J Clin Ultrasound 1997; 25:378–82.[Medline]

10. Stratton JF, Ni Scanaill S, Stuart B, Turner MJ. Are babies of normal birth weight who fail to reach their growth potential as diagnosed by ultrasound at increased risk? Ultrasound Obstet Gynecol 1995; 5:114–8.[Medline]

11. Turner MJ, Rasmussen MJ, Turner JE, Boylan PC, MacDonald D, Stronge JM. The influence of birth weight on labor in nulliparas. Obstet Gynecol 1990;76:159–63.[Abstract/Free Full Text]

12. Ott WJ. Sonographic diagnosis of intrauterine growth restriction. Clin Obstet Gynecol 1997;40:787–95.[Medline]

13. Danielian PJ, Allman AC, Steer PJ. Is obstetric and neonatal outcome worse in fetuses who fail to reach their own growth potential? Br J Obstet Gynaecol 1992;99:452–4.[Medline]

14. Lockwood CJ, Weiner S. Assessment of fetal growth. Clin Perinatol 1986;13:3–35.[Medline]

15. Patterson RM, Pouliot RN. Neonatal morphometrics and perinatal outcome: Who is growth retarded? Am J Obstet Gynecol 1987;157: 691–3.[Medline]





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