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  Subcutaneous Fat in the Fetal Abdomen as aPredictor of Growth Restriction FRANC¸OIS GARDEIL, MRCOG, RICHARD GREENE, MRCOG,BERNARD STUART, FRCOG, AND MICHAEL J. TURNER, FRCOG Objective : To determine if measuring fetal abdominal fatantenatally using ultrasound can predict fetal growth restric-tion (FGR).  Methods : One hundred thirty-seven unselected womenwith singleton pregnancies had serial ultrasound scans at 20,26, 31, and 38 weeks’ gestation. Subcutaneous fat in the fetalabdomen was measured using the same section as theabdominal circumference (AC). Outcome measures werebirth weight, neonatal morbidity, and ponderal index. Results : Infants with subcutaneous fat less than 5 mm at38 weeks ( n  51) were almost five times more likely to havea birth weight below the 10th centile than those withsubcutaneous fat of 5 mm or more ( n  75). The incidence ofneonatal morbidity was significantly higher in infants withsubcutaneous fat less than 5 mm, compared with those withsubcutaneous fat of 5 mm or more (20% versus 8%,  P  <<< .05).Decreased subcutaneous fat was also associated with a highprevalence of low ponderal index, regardless of birth weightcategory. Conclusion : Measurement of fat in the abdominal wall is asimple technique with a sensitivity for predicting low birthweight similar to that of conventional sonography and mightpotentially predict FGR irrespective of fetal weight. (ObstetGynecol 1999;94:209–12. © 1999 by The American Collegeof Obstetricians and Gynecologists.) Fetal growth restriction (FGR) might be defined as thesuppression of genetic growth potential that occurs inresponse to impaired nutrient oxygen supply to thefetus. It is a cause of perinatal death and is associatedwith significant neonatal morbidity. Adaptation to alimited supply of intrauterine nutrient might increasethe risk of coronary heart disease, hypertension, andinsulin resistance in later life. 1,2 Severe FGR often results in births of infants whoweigh less than the 10th centile for gestation. Themajority of small infants, however, are well nourished.Evidence of FGR can be found in infants of apparentlynormal weight. 3 The statistical classification of infantsinto weight centile categories 4 has limited value in theassessment of fetal nutrition.Antenatal diagnosis of FGR remains a challenge.Ultrasonography is the best technique, estimating fetalweight and growth velocity using multiple parameters.Body proportionality indices such as ratio of head-to-abdominal circumference 5 and Doppler ultrasoundstudies 6 can provide additional information. Diagnosisis easier at birth because growth-restricted infants showtypical changes in body proportionality. Subcutaneousadipose tissue that acts as an energy source and insu-lator against hypothermia is reduced. 7 Subcutaneous fat, which can be evaluated by meansof skinfold thickness, can be seen antenatally withultrasound. On a transverse section of the fetal abdo-men, it appears as a well-delineated echogenic line andhas been described previously by two investigators. 8,9 We conducted a prospective study involving serialmeasurements of subcutaneous fat in the abdominalwall to determine whether it could predict FGR.  Material and Methods Beginning in November 1996, we invited all womenpresenting for their first antenatal visits at the CoombeWomen’s Hospital to participate in our study by havingserial ultrasound scans at 20, 26, 31, and 38 weeks’gestation. However, enrollment was limited to 12 perweek. The volunteers gave informed consent and hadearly sonographic confirmation of dates, and multiplepregnancies were excluded. Scans were done by twooperators (FG and RG) with an Ultramark 4 PlusUltrasound System (Advanced Technology Laborato-ries, Bothell, WA). Standard sections used for abdomi-nal circumference (AC) were obtained, and subcutane-ous fat in abdominal walls was measured in millimeterson the anterior abdominal wall, anterior to the marginsof the ribs, using magnification (Figure 1). Biparietal From the Coombe Women’s Hospital, Dublin, Republic of Ireland. 209 VOL. 94, NO. 2, AUGUST 1999 0029-7844/99/$20.00PII S0029-7844(99)00270-7  diameter (BPD), occipitofrontal diameter, head circum-ference (HC), and AC and femur length (FL) were alsomeasured routinely. With the exception of subcutane-ous fat, all the sonographic findings were reported toclinicians caring for the women.By December 1997, 137 women had delivered. Thisstudy group was similar to the hospital population. Allwomen but one were Irish. The mean age was 29 years.Forty-one percent of the women were nulliparous. Wealso selected 24 women (six at each gestation) to assessinterobserver reproducibility. The two operators madethe same measurements in 23 cases. Outcome measureswere birth weight, weight-to-length ratio (ponderalindex in kg/m 3 ), and perinatal outcome. For birthweights we used our own hospital centiles. 10 We de-fined two groups of infants at follow-up, those withsubcutaneous fat thickness of less than 5 mm at 38weeks and those with 5 mm or more. Between-groupdifferences in rates of morbidity and incidence of lowponderal index were tested for significance by    2 anal-ysis. A statistical significance level of   P    .05 wasaccepted. Results Table 1 shows the subcutaneous fat measurementsmade during the study. At 20 weeks’ gestation, thelayer of subcutaneous fat could only be identified in 102of 137 fetuses. Eleven women (8%) delivered before 38weeks. The range and mean of subcutaneous fat mea-surements increased with gestation. Sixty-two womendelivered between 38 and 40 weeks’ gestation. Theremaining 64 women delivered between 40 and 42weeks.Table 2 shows the birth weight centiles for gestationalage using a cutoff point of 5 mm at 38 weeks’ gestation.Of the 51 infants with subcutaneous fat thickness of lessthan 5 mm, 16 (31.4%) weighed less than the 10thcentile. Only 5 (6.7%) of 75 infants with measurementsof 5 mm or more weighed less than the 10th centile. Asubcutaneous fat thickness of less than 5 mm at 38weeks had a sensitivity of 76.2% (16 of 21) and aspecificity of 66.6% (70 of 105) for predicting birthweight below the 10th centile. Ultrasound estimation of fetal weight, based on standard biometry parameters at38 weeks, had a sensitivity of 80.1% and a specificity of 96% for predicting birth weight below the 10th centilein this series. An infant with subcutaneous fat of lessthan 5 mm was almost five times more likely to have birth weight below the 10th centile than was an infantwith subcutaneous fat of 5 mm or more. None of the 33infants with subcutaneous fat of 6 mm or more had birth weights below the 10th centile.There were no perinatal deaths. Table 3 shows neo-natal morbidity. The incidence of neonatal morbiditywas significantly higher in infants with subcutaneousfat of less than 5 mm ( P  .05). There was no morbidityamong the five infants who weighed less than the 10thcentile who had subcutaneous fat thickness of 5 mm ormore at 38 weeks.We determined ponderal index, based on accuratecrown–heal length measured at birth, for 99 of 126infants delivered after 38 weeks. Of those 99 infants, 45had subcutaneous fat of less than 5 mm at 38 weeks and54, subcutaneous fat of 5 mm or more. The prevalenceof low ponderal index (less than 24 kg/m 3 ) was higher Figure 1.  Measurement of subcutaneous fat in the fetal abdomen. Table 1.  Measurements of Subcutaneous Fat Gestation(wk)Subcutaneous fat (mm)1 2 3 4 5 6 7 8 920 ( n  102) 20 70 12 0 0 0 0 0 026 ( n  137) 3 44 64 23 3 0 0 0 031 ( n  137) 0 11 51 57 17 1 0 0 038 ( n  126) 0 1 13 37 42 25 6 1 1 Table 2.  Birth Weight Centiles According to SubcutaneousFat Thickness at 38 Weeks Birth weightcentilesFat  5 mm( n  51)Fat  5 mm( n  75)1–9 16 510–19 8 520–29 5 230–39 2 540–49 2 1150–59 6 660–69 5 870–79 3 880–89 2 1290–99 2 13 210 Gardeil et al  Fat in Fetal Abdomen Obstetrics & Gynecology  among infants with fat of less than 5 mm than thosewith 5 mm or more (20% versus 5%,  P  .05).Although the thickness of subcutaneous fat increasedwith gestation in the majority of cases, nine infants inour study had measurements lower at 38 than at 31weeks’ gestation. Three of the nine, who all had subcu-taneous fat less than 5 mm at 38 weeks, weighed belowthe 10th centile and had ponderal indices of less than 24kg/m 3 . The other six infants had a birth weights withinnormal range. Four had ponderal indices calculated,which were less than 24 kg/m 3 in three cases. The threeinfants with low ponderal indices and birth weightsabove the 10th centile had neonatal morbidity. Discussion Assessment of fetal size and growth is important forantenatal care. It is hoped that early recognition of anabnormality, appropriate surveillance, and interventionwill optimize perinatal outcomes. Although duration of labor and the need for operative delivery for dystociaincrease with fetal weight, 11 obstetricians concentrateon identifying small-for-gestational-age fetuses. Thediagnostic value of conventional ultrasound for detect-ing small infants is established, with varying degrees of predictive ability quoted for different ultrasound pa-rameters. 12 Our study showed a thin layer of subcuta-neous fat at 38 weeks’ gestation associated with low birth weight. Using a cutoff point of 5 mm, we coulddetect 76.2% of infants who weighed less than the 10thcentile at birth. Although sensitivity of measurementscompared favorably with conventional ultrasound bi-ometry, specificity and predictive values were low.Measurement of subcutaneous fat in the fetal abdomi-nal wall cannot replace sonographic estimation of fetalweight; however, it is a simple and fast technique thatcould be used as a screening test and might comple-ment existing sonographic parameters.Growth restriction, with its metabolic complications,can be found in infants of normal weight, 3,13 and themajority of small infants are not growth restricted, sothere is a need to evaluate characteristic that mightpredict nutrition status beyond birth weight. Protein–calorie deprivation results in soft-tissue wasting withrelatively spared skeletal growth. The ponderal index, 14 a weight-to-height ratio that shows this asymmetry, is arecommended outcome measure for studies on growthrestriction. 7 A low ponderal index in neonates is a majorpredictor of poor outcomes. 15 Our results show thatsubcutaneous fat of less than 5 mm at 38 weeks’gestation appears to associate with low ponderal indexat birth. Our study showed that the incidence of neo-natal morbidity was significantly higher in infants witha subcutaneous fat of less than 5 mm at 38 weeks,compared with infants with a subcutaneous fat of 5 mmor more. A decrease in subcutaneous fat thickness in thethird trimester was also associated with a high inci-dence of low ponderal index and neonatal morbidity.This study raises the exciting possibility that mea-surement of subcutaneous fat in the abdominal wallmight help predict nutrition status antenatally, irrespec-tive of weight. That could minimize unnecessary obstet-ric intervention for small, well-nourished fetuses anddetect true FGR in infants of apparently normal weight,a high-risk group rarely identified with current meth-ods of antenatal care. A larger study will be necessary todetermine the independent predictive power of mea-surement of subcutaneous fat in the fetal abdomen. References 1. Barker DJ. The long-term outcome of retarded fetal growth. ClinObstet Gynecol 1997;40:853–63.2. Martyn CN, Barker DJ, Osmond C. Mothers’ pelvic size, fetalgrowth, and death from stroke and coronary heart disease in menin the UK. Lancet 1996;348:1264–8.3. Chard T, Costeloe K, Leaf A. Evidence of growth restriction inneonates of apparently normal weight. Eur J Obstet GynaecolReprod Biol 1992;45:59–62.4. Battaglia FC, Lubchenco LO. A practical classification of newborninfants by birth weight and gestational age. J Pediatr 1967;71:159–63.5. Campbell S, Thoms A. Ultrasound measurement of the fetal headto abdomen circumference ratio in the assessment of growthretardation. Br J Obstet Gynaecol 1977;84:165–74.6. Stuart B, Drumm J, Fitzgerald DE, Duignan NM. Fetal bloodvelocity waveforms in normal pregnancy. Br J Obstet Gynaecol1980;87:780–5.7. Beattie RB, Johnson P. Practical assessment of neonatal nutritionstatus beyond birthweight: An imperative for the 1990s. Br J ObstetGynaecol 1994;101:842–6.8. Hill LM, Guzick D, Boyles D, Merolillo C, Ballone A, Gmiter P.Subcutaneous tissue thickness cannot be used to distinguish ab-normalities of fetal growth. Obstet Gynecol 1992;80:268–71.9. Petrikovsky BM, Oleschuk C, Lesser M, Gelertner N, Gross B.Prediction of fetal macrosomia using sonographically measuredabdominal subcutaneous tissue thickness. J Clin Ultrasound 1997;25:378–82.10. Stratton JF, Ni Scanaill S, Stuart B, Turner MJ. Are babies of normal birth weight who fail to reach their growth potential as diagnosed Table 3.  Subcutaneous Fat Thickness at 38 Weeks andNeonatal Morbidity Fat  5 mm( n  51)Fat  5 mm( n  75)Meconium aspiration 1 0Hypoglycemia 5 2Hypothermia 3* 1Poor feeding 2* 0 Jaundice 1 310 (20%) 6 (8%)* One infant had hypoglycemia and hypothermia. One had hypo-glycemia and poor feeding. VOL. 94, NO. 2, AUGUST 1999  Gardeil et al  Fat in Fetal Abdomen  211   by ultrasound at increased risk? Ultrasound Obstet Gynecol 1995;5:114–8.11. Turner MJ, Rasmussen MJ, Turner JE, Boylan PC, MacDonald D,Stronge JM. The influence of birth weight on labor in nulliparas.Obstet Gynecol 1990;76:159–63.12. Ott WJ. Sonographic diagnosis of intrauterine growth restriction.Clin Obstet Gynecol 1997;40:787–95.13. Danielian PJ, Allman AC, Steer PJ. Is obstetric and neonataloutcome worse in fetuses who fail to reach their own growthpotential? Br J Obstet Gynaecol 1992;99:452–4.14. Lockwood CJ, Weiner S. Assessment of fetal growth. Clin Perinatol1986;13:3–35.15. Patterson RM, Pouliot RN. Neonatal morphometrics and perinataloutcome: Who is growth retarded? Am J Obstet Gynecol 1987;157:691–3. Address correspondence and reprint requests to: Franc¸ois Gardeil, MRCOGCoombe Women’s HospitalDublin 8, Republic of IrelandE-mail: gardeil@iol.ie Received October 2, 1998.Received in revised form January 25, 1999. Accepted February 10, 1999. Copyright © 1999 by The American College of Obstetricians andGynecologists. Published by Elsevier Science Inc. 212 Gardeil et al  Fat in Fetal Abdomen Obstetrics & Gynecology
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