Fetal Echogenic Gut: a Marker of Intrauterine Gut Arch Dis Child: First Published As 10.1136/Adc.69.5 Spec No.510 on 1 November 1993

510 Archives ofDisease in Childhood 1993; 69: 510-513

Fetal echogenic gut: a marker of intrauterine gut Arch Dis Child: first published as 10.1136/adc.69.5_Spec_No.510 on 1 November 1993. Downloaded from ischaemia?

A K Ewer, J M McHugo, S Chapman, S J Newell

Abstract When FEG is observed in the fetus with The pathophysiological significance of IUGR, problems with enteral feeding fetal echogenic gut (FEG) is unknown. should be anticipated. Our aim was prospectively to evaluate (Arch Dis Child 1993; 69: 510-513) FEG in infants with intrauterine growth retardation (IUGR) and absent umbilical artery end diastolic flow velocities. Over a Fetal assessment is providing an increasing 15 month period, nine infants with FEG amount of information about preterm infants met these criteria. Nine infants who, on before they arrive on the neonatal intensive antenatal assessment, had demonstrated care unit. The finding of hyperechogenic gut IURG and absent umbilical artery end on antenatal ultrasound has been described diastolic flow velocities, but no evidence previously. Intra-abdominal calcification and of FEG, were selected as case-controls. echogenic ascites secondary to meconium peri- Gastrointestinal function was then tonitis are well documented,' and Blott et al prospectively evaluated in both groups described hyperechogenic gut in eight fetuses after delivery. who subsequently developed obstruction due All liveborn infants received nasogastric to meconium without intestinal perforation.2 feeds of breast milk by 8 days of age. All In this study FEG was defined as a generalised in the FEG group developed marked increase in the echogenicity of the bowel, with- abdominal distension, large, bile stained, out evidence of ascites, in a fetus who is other- nasogastric aspirates, and constipation wise structurally normal. requiring rectal washouts. This led to a During detailed assessment of 'at risk' discontinuation of enteral feeds on one or fetuses we have observed hyperechogenic or Birmingham more occasions. Two patients in the FEG 'bright' gut (FEG) on ultrasound scan in a Maternity Hospital group required water soluble contrast number of growth retarded fetuses with absent A K Ewer enemas in order to relieve intestinal umbilical artery end diastolic flow velocities.3 J M McHugo obstruction. In the control group, 3/9 In the growth retarded infant with abnormal Birmingham patients had abdominal distension, but no antenatal Doppler studies, an increased inci- Children's Hospital rectal washouts were given and enteral dence of necrotising enterocolitis has been S Chapman 5 feeds were not interrupted. The median demonstrated.4 It is possible that regional http://adc.bmj.com/ Institute of Child (range) time to tolerate full enteral feeds redistribution of blood flow may lead to Health, University of was 15 (7-32) days in the FEG group, com- chronic hypoperfusion of the gut and the Birmingham S J Newell pared with 4 (1-8) days in the control echogenicity noted may be a marker of this group. In the FEG group 5/6 patients phenomenon. We therefore hypothesised that Correspondence to: Dr S J Newell, Regional required parenteral nutrition for 5-27 the gastrointestinal function may be affected in Neonatal Intensive Care days. In the control group one patient infants who demonstrated FEG. The aim of Unit, St James's University nutrition over a this study was prospectively to evaluate gas- Hospital, Beckett Street, required parenteral on October 1, 2021 by guest. Protected copyright. Leeds LS9 7TF. period of four days only. No child had trointestinal function in patients with FEG and Accepted 18 May 1993 necrotising enterocolitis or cystic fibrosis. matched case controls.

7, --, L'06 .4- B':: ...- L,;.:--,n.--, 'I.: Patients and methods FEG was detected on antenatal ultrasound and -0-- dit"-WW was defined as an abnormally bright area of bowel which had a similar echogenicity to the fetal vertebral body (fig 1). Over a 17 month period at Birmingham Maternity Hospital, during ultrasonic assessment of high risk pregnancies, fetuses with intrauterine growth retardation (IUGR, defined as abdominal circumference less than the 5th centile on one or more occasions), and absent umbilical artery end diastolic flow velocities on Doppler ultrasound, were examined for the presence of FEG. Fetal ultrasonography, Doppler studies, and assessment of gut echogenicity were all performed by the same observer (JMM). Nine 1 Two the same The normal ultrasonic Figure ultrasound imagesfrom fetus. (A) were in whom this appearance of thefetal abdomen. (B) Three weeks later showing the presence ofFEG. The fetuses with FEG identified, abnormally bright area of bowel is arrowed; V. vertebral body, F: femur. was the only ultrasonic abnormality. FEG was Fetal echogenic gut: a marker ofintrauterine gut ischaemia? 511

1 Table Clinical characteristics ofinfants with FEG Results Arch Dis Child: first published as 10.1136/adc.69.5_Spec_No.510 on 1 November 1993. Downloaded from Birth Head Birthweight Three patients with FEG were stillborn and Gestation weight circumference SD score IPPV Maternal detailed postmortem examination performed (weeks) Sex (g) (cm) (SD) Outcome (days) factors by the regional perinatal pathologist revealed 29 M 1160 28-5 -0 77 Alive 7 Pre-eclampsia no abnormality, other than maceration, in the 29 M 620 22-0 -3-74 Alive 18 Abnormal gastrointestinal tract. One infant in the control __ _ cardiotocograph 35 F 770 25-1 -3-84 Alive 0 group died at 8 days of age from intracranial 30 F 810 24-5 -2-70 Alive 0 Abnormal cardiotocograph haemorrhage. All liveborn infants were small 29 F 640 24-5 -3-63 Stillbom for gestational age. Three infants from the 30 F 900 25-5 -2-34 Stillbom Oligohydramnios FEG group and four from the control group 29 M 770 25-0 -2-91 Alive <1 Abnormal cardiotocograph required mechanical ventilation, but none had 32 M 790 25-0 -4-43 Alive 0 severe lung disease (tables 1 and 2). 28 F 640 21-0 -3-12 Stillborn All infants received, in the first instance, IPPV: intermittent positive pressure ventilation. expressed breast milk as hourly bolus nasogastric feeds and there was no significant dif- first detected at between 18 and 30 weeks' ges- ference between the two groups in the timing tation. The precise timing of the onset of FEG of the introduction of feeds. In all six surviving was difficult to evaluate in all patients because infants in the FEG group, difficulties were several were transferred from other centres late encountered introducing enteral feeds. Milk in pregnancy for further assessment. was introduced at a median of 2 days of age FEG was noted consistently in four patients with a range of 1-8 days. All six infants were on at least two occasions. In two of these noted by nursing staff to develop marked patients it was demonstrated at 18 weeks and abdominal distension and large, bile stained, persisted until delivery at 29 and 35 weeks. In nasogastric aspirates (greater than 80% of the the other two FEG was first seen at 21 and 27 total feed given over the previous four hours) weeks and persisted until 24 and 29 weeks' or vomits were obtained shortly after introduc- gestation respectively. Among the remaining tion of feeds. This resulted in discontinuation five patients, it was observed one week before of feeds for a minimum of 24 hours on at least delivery in two, and in three cases on the day of one occasion in each case; feeds were discon- delivery during the first scan at Birmingham tinued on two occasions in three infants and on Maternity Hospital after in utero transfer. three occasions in one infant. Once noted FEG did not resolve in any of There was difficulty or a delay passing the patients and clinical data were then meconium in all infants with FEG. Although recorded prospectively on each infant follow- three patients in this group passed meconium ing delivery (table 1). Three of the FEG group within 24 hours of birth, two of the three were stillborn and postmortem examination required glycerine suppositories in order to was performed in each case. Each infant with achieve this. In three patients, meconium FEG was then matched for gestational age and passage was delayed beyond 24 hours (25, 43, birth weight with the next consecutively avail- and 90 hours), and glycerine suppositories able infant who fulfilled the entry criteria: were again required. Despite the subsequent

IUGR as defined above, and absent umbilical administration of suppositories to all six infants http://adc.bmj.com/ artery end diastolic flow velocities (table 2). with FEG, this resulted in the passage of small None ofthe case controls had FEG. There was amounts of meconium only, which was insuffi- no significant difference between the two cient to relieve the abdominal distension. All groups in gestation, birth weight, head circum- infants went on to receive saline or acetylcys- ference, birthweight SD score, or sex ratio teine rectal washouts at intervals of six hours. (Mann-Whitney U analysis). In four infants this was sufficient and was Gastrointestinal function was evaluated in followed by adequate passage of meconium each infant according to the following criteria: and relief of the abdominal distension. Two on October 1, 2021 by guest. Protected copyright. presence of abdominal distension, delay or infants continued to have problems despite difficulty in the passage of meconium, time to rectal washouts and became clinically full enteral feeds, and necessity for parenteral obstructed with dilated bowel loops radio- nutrition. logically. Water soluble contrast enemas (Urografin 150, Schering Health Care Limited) were employed to relieve the obstruc- Table 2 Clinical characteristics ofcase-control infants tion (fig 2). In the first patient the enema revealed a microcolon with small meconium Birth Head Birthweight Gestation weight circumference SD score IPPV Maternal plugs in the distal colon and more compacted (weeks) Sex (g) (cm) (SD) Outcome (days) factors plugs in the proximal colon. Contrast medium 32 M 1465 29-0 -1-78 Alive 0 Pre-eclampsia could not be encouraged into the terminal 31 M 765 24-0 -3-01 Alive 0 ileum during the first enema, but at a second 32 F 700 24-0 -4-78 Alive 2 Abnormal cardiotocograph enema 24 hours later, contrast medium passed 31 M 935 25-0 -2-46 Alive 0 Pre-eclampsia into dilated loops of terminal ileum containing 31 F 545 22-3 -3-71 Neonatal death 8 meconium plugs. Large amounts of meconium 31 F 1240 28-0 -1-48 Alive 0 were passed. In the second patient two water 29 M 925 26-0 -2-06 Alive 4 Abnormal cardiotocograph soluble contrast enemas were given over a 24 36 F 1610 31-0 -2-42 Alive 0 Pre-eclampsia hour period. Multiple plugs of meconium 28 M 880 26-0 -1-56 Alive 10 Abnormal cardiotocograph plugs filled a normal calibre colon and distal ileum (fig 2). At the first attempt contrast IPPV: intermittent positive pressure ventilation. medium did not pass beyond the terminal 512 Ewer, McHugo, Chapman, Newell

All infants subsequently tolerated feeds Arch Dis Child: first published as 10.1136/adc.69.5_Spec_No.510 on 1 November 1993. Downloaded from B satisfactorily and had no further gastrointestinal problems during their stay on the neonatal unit. No infant developed necrotising enterocolitis and none of the infants had abnormal immune reactive trypsin or clinical features to suggest cystic fibrosis.

Discussion There is now ample evidence to suggest that intrauterine growth retardation is strongly associated with increased perinatal mortality6 and neonatal morbidity7 and, in survivors, long term handicap.8 Doppler ultrasound technology has made it possible to study the flow characteristics of the fetal circulation and over the past decade many data have been reported that link reduced Figure 2 (A) Abdominal radiograph showing multiple dilated bowel loops. (B) Contrast diastolic flow velocity in the umbilical artery study in same patient showing normal calibre colon and distal ileum containing multiple with growth retardation.9-11 The abnormal flow meconium plugs (arrowed). velocity is associated with an obliteration of small arteries in the tertiary villi of the placenta, ileum but did facilitate the passage of some thus increasing the placental resistance.12 meconium. The second enema revealed that Comparison studies ofDoppler velocities ofthe much of the meconium had passed and con- umbilical and carotid arteries of normal and trast medium flowed beyond the meconium growth retarded fetuses show a 'brain sparing' plugs into air-containing ileum. effect in the more compromised growth In the control group, feeds were introduced retarded group,13 14 suggesting a redistribution at a median of 1 day with a range of 1-3 days. of regional blood flow in order to maintain Two patients did not pass meconium within 24 optimal oxygen supply to the fetal brain. The hours of birth (27 and 34 hours) and three beneficial effects of the relative increase in infants had mild abdominal distension but cerebral blood flow may be offset by a poten- these symptoms responded to administration tially detrimental effect on other vascular beds, of glycerine suppositories and no baby including the splanchnic circulation. required a rectal washout. Feeds were not Recent reports have also suggested an interrupted. association between very abnormal umbilical Mean time to full enteral feeds and need for artery Doppler studies which show absent or parenteral nutrition differed markedly between reversed end diastolic flow velocities and neo- the FEG group and the controls. Full enteral natal morbidity including an increased inci-

feeds, defined as daily fluid requirement given dence of necrotising enterocolitis.4 5 This may http://adc.bmj.com/ enterally without the need for intravenous sup- be related to an ischaemic insult to the gut. plementation, were established by a median of Although intrauterine assessment of gut per- 15 days in the FEG group with the range of fusion is technically very difficult it may be 7-32 days, compared with a median of 4 days postulated that in the growth retarded fetus (range 1-8) in the control group (fig 3). Five of with abnormal end diastolic flow velocities the the infants in the FEG group required splanchnic circulation is compromised in nutrition for a median of 15 days favour of the cerebral circulation and in some parenteral on October 1, 2021 by guest. Protected copyright. with a range of 5-27 days compared with one cases it is possible that the gut may suffer from of the control group who required parenteral chronic hypoperfusion. nutrition for four days only. The differences In the normal infant we have observed between the two groups in time to full enteral hyperechoic areas in the peritoneal cavity as feeds and duration of parenteral nutrition were a transient phenomenon during the second highly significant using Mann-Whitney U trimester. In infants with gastrointestinal analysis (p

haemorrhage, and neonatal morbidity. BMJ 1987; 294: be successfully managed with rectal washouts Arch Dis Child: first published as 10.1136/adc.69.5_Spec_No.510 on 1 November 1993. Downloaded from 13-6. or, ifnecessary, water soluble contrast enemas. 6 Tejani N, Mann L. Diagnosis and management of the small Noting the gut in infants with for gestational age fetus. Clin Obstet Gynecol 1977; 20: dysfunction 943-55. FEG, we may speculate that FEG is a reflec- 7 Dobson PC, Abell DA, Beisher NA. Mortality and morbid- tion of gut abnormality, perhaps ischaemia. ity of fetal growth retardation. Aust N ZJ Obstet Gynaecol 1981; 21: 69-72. This may occur as a result of redistribution of 8 Commey JOO, Fitzhardinge PM. Handicap in the preterm regional blood flow in the compromised fetus. small for gestational age infant. Jf Pediatr 1979; 94: 779-86. This results in initial problems with passage of 9 Fleischer A, Shulman H, Farmakides G, Bracero L, Blattner meconium and may adversely affect gut P, Randolph G. Umbilical artery velocity waveforms and intrauterine growth retardation. Am Jf Obstet Gynecol motility. 1985; 151: 502-5. 10 Erskine RLA, Ritchie JWK. Umbilical artery blood flow characteristics in normal and growth retarded fetuses. BrJ 1 Foster MA, Nyberg DA, Mahony BS, Mack LA, Marks Obstet Gynaecol 1985; 92: 605-10. WM, Raabe RD. Meconium peritonitis: prenatal sono- 11 Reuwer PJHM, Bruinse HW, Stoutenbeek P, Haspels AA. graphic findings and their clinical significance. Radiology Doppler assessment of the feto-placental circulation in 1987; 165: 661-5. normal and growth retarded fetuses. Eur Jf Obstet Gynecol 2 Blott M, Greenough A, Gamsu HR, Nicolaides K, Reprod Biol 1984; 18: 199-205. Campbell S. Antenatal factors associated with obstruction 12 Giles WB, Trudinger BJ, Baird PJ. Fetal umbilical artery of the gastrointestinal tract by meconium. BMJ 1988; flow velocity waveforms and placental resistance: 296: 250. pathological correlation. Br Jf Obstet Gynaecol 1985; 92: 3 Trudinger BJ, Giles WB, Cook CM, Bombardieri J, Collins 31-8. L. Fetal umbilical artery flow velocity waveforms and 13 Wladimiroff JW, Noordam MJ, van den Wijngaard JAGW, placental resistance: clinical significance. Br Jf Obstet Hop WCJ. Fetal internal carotid and umbilical artery Gynaecol 1985; 92: 23-30. blood flow velocity waveforms as a measure of fetal well- 4 Malcolm G, Ellwood D, Devonald K, Beilby R, Henderson- being in intrauterine growth retardation. Pediatr Res 1988; Smart D. Absent or reversed end diastolic flow velocity in 24: 609-12. the umbilical artery and necrotising enterocolitis. Arch Dis 14 Wladimiroff JW, van den Wijngaard JAGW, Degani S, Child 1991; 66: 805-7. Noordam MJ, van Eyck J, Tonge HM. Cerebral and 5 Hackett GA, Campbell S, Gamsu H, Cohen-Overbeek T, umbilical arterial blood flow velocity waveforms in normal Pearce JMF. Doppler studies in the growth retarded fetus and growth-retarded pregnancies. Obstet Gynecol 1987; and prediction of neonatal necrotising enterocolitis, 69: 705-9. http://adc.bmj.com/ on October 1, 2021 by guest. Protected copyright.