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Abnormal antepartum fetal heart rate patterns and subsequent handicap

G. H. A. VISSER

Antepartum fetal heart rate (FHR) monitoring is widely used to evaluate the fetal condition in utero. With this technique it is mainly the state of oxygenation of the fetus that is assessed. Thus, in studying the relationship between abnormal antepartum FHR traces and subsequent handicap, the effect ofantepartum hypoxaemia (and acidaemia) on outcome is investigated. As most FHR abnormalities occur in intrauterine growth-retarded (IUGR) fetuses, effects of hypoxaemia will undoubtedly be mixed with those of a poor supply of other nutrients.

In this paper data on abnormal antepartum FHR patterns are related to the state of fetal oxygenation and to neurological outcome with special emphasis on the IUGR fetus. Secondly, data are reviewed on heart rate patterns of congenitally abnormal fetuses and fetuses who acquire severe brain damage in utero. In these cases heart rate abnormalities are presumably a direct expression of nervous system abnormality.

FHR AND OXYGENATION

In IUGR fetuses antenatal FHR patterns will usually be found to be normal (Visser, 1984). The first abnormalities that occur with progressive deterio- ration of the fetal condition are late heart rate decelerations ('decelerative' pattern). The latter coincide with a low Po2 in the umbilical arteries and vein ('hypoxaemia') at elective caesarean section (Bekedam et al, 1987). Acidaemia is usually absent and will only be found with a so-called 'terminal' FHR pattern, which is a completely 'flat' tracing with shallow late decelerations (Bekedam et al, 1987; Visser et al, 1980). Heart rate variation, the incidence of accelerations and that of gross body movements fall below the normal range at about the same time as late decelerations occur (Bekedam et al, 1987). The temporary decrease of heart rate variation and of movements directly after 'hypoxaemic' events (late decelerations) and the increase during maternal hyperoxygenation further indicate the relationship of these two variables with the oxygenation status of the fetus (Bekedam and Visser, 1985; Bekedam et al, 1986).

Baillikre's Clinical Obstetrics and Gynaecology--VoL 2, No. 1, March 1988 117

1 18 G.H.A. VISSER

These data indicate that in I U G R fetuses antepartum F H R changes are rather late signs of impairment. The first abnormalities that occur (late decelerations) coincide with fetal hypoxaemia. In the rhesus monkey it was also found that with progressive deterioration in fetal condition the first sign is the appearance of late decelerations. In this animal this situation was also associated with fetal hypoxaemia (Murata et al, 1982). In growth-retarded fetal sheep a low arterial Po2 can sometimes be present for weeks before acidaemia and finally intrauterine death occur (Robinson et al, 1985). The presence of chronic hypoxaemia has recently been confirmed in I U G R human fetuses in which blood sampling was performed by cordocentesis (Soothill et al, 1987). Decelerative and terminal F H R patterns observed antepartum are likely to indicate chronic hypoxaemia and acidaemia, respectively.

FHR AND BRAIN ABNORMALITIES

Although antepartum FHR monitoring is mainly used to assess the state of oxygenation, F H R abnormalities may also indicate brain abnormality. This has been shown in studies of anencephalic fetuses (de Haan et al, 1971; Terao et al, 1984). An intact hind-brain and medulla oblongata are essential for heart rate accelerations to occur, whereas the cortex is necessary for the cyclic appearance of episodes of high and low heart-rate variability. In anencepha- lics with only part of the spine present the fetal heart rate pattern is 'flat', with occasional V-shaped decelerations.

A persistent f ixed--or f l a t - -FHR pattern has been shown to follow decerebration in fetal sheep (Dawes et al, 1983) and in the neonate this phenomenon can be considered one of the criteria of brain death (Kero et al, 1978). It may also be the consequence of acquired brain damage in utero. Fricker et al (1983) reported on a term fetus with a persistent flat F H R pattern antepartum. During labour the scalp pH was normal. The newborn infant showed severe neurological abnormalities and as early as the first day of life a CT scan showed extensive hypodense zones. Based on the course of the CT scan changes it was assumed that the 'hypoxic' insult had occurred some days prior to the onset of labour. In this case the brain damage was probably caused by a transitory occlusion of the umbilical cord. In another case a flat F H R pattern followed a temporal maternal respiratory and cardiovascular collapse (van der Moer et al, 1985). This infant was born three weeks later with porencephaly of the cerebrum and brain stem. In a third case, in which serious cerebrospinal lesions were also preceded by a fixed F H R pattern antepartum, no cause of the lesions could be determined (Adams et al, 1977).

Recent literature indicates that central nervous system injuries occurring prior to the labour process are not rare (Barth, 1984; Sims et al, 1985; Paul et al, 1986; Mann, 1986). The causes include respiratory and circulatory accidents to the mother, abdominal trauma during pregnancy, twin preg- nancy with a macerated co-twin, arterial occlusion of fetal cerebral vessels, placental insufficiency and infections (Barth, 1984; Sims et al, 1985). At post mortem cerebral haemorrhage, gliosis or porencephaly are found. Porence- phaly may also be the result of genetic diseases (Barth, 1984). Up until now

FETAL H E A R T RATE P A T T E R N S A N D H A N D I C A P 119

many of the surviving infants with such injuries have probably been left with 'unexplained' neurological handicaps, or handicaps thought to be due to the labour process. Antepartum FHR monitoring and prenatal ultrasound examinations might identify these cases and distinguish them from abnor- malities of the nervous system acquired during and after birth.

FHR AND NEUROLOGICAL MORBIDITY

There are only a few studies concerning the relationship between antepartum FHR abnormalities and neurological outcome. Unfortunately all but one suffer from the fact that part of the population was allowed to go into labour. This makes it difficult to determine if outcome is related to antepartum complications and/or to problems induced by the process of labour.

We investigated the relationship between antepartum FHR patterns and neonatal neurological morbidity in 23 small-for-dates (SFD) full-term infants and in 33 SFD infants delivered before 37 weeks (Dijxhoorn, 1986; Dijxhoorn et al, 1987). All subjects were selected from the database of the Groningen Perinatal Project, containing prenatal and perinatal data on 3162 children from consecutive singleton pregnancies, all surviving the neonatal period. Details of the obstetrical-neonatal neurological relationship of the total study population have been published before (Jurgens-van der Zee et al, 1979; Huisjes et al, 1980). Selection for the current study in SFD infants depended upon the availability of umbilical blood gas values at birth. A standardized neonatal neurological examination (Prechtl, 1977) was performed during the neonatal period; infants born prematurely were examined at term. The results were expressed in a neurological classification (normal, suspect, abnormal) and in a neonatal neurological optimality score (NNOS, range 0-60; Touwen et al, t980).

The results are summarized in Table 1. All but six of the fetuses with decelerations were delivered by elective caesarean section (CS): in the term group there were three with a normal antepartum FHR pattern but with decelerations in early labour who were eventually delivered by secondary CS; in the preterm group three fetuses with decelerations were delivered vaginally.

There was a strong correlation between heart rate decelerations (of which 80% occurred antenatally and the remainder in early labour) and neonatal neurological morbidity. Neurologically 'abnormal' infants were restricted to the group with decelerations, with poorest outcome in the subgroup with a 'terminal' antepartum FHR pattern. There was also a good correlation between the umbilical artery pH and neurological morbidity. No relationship between pH and morbidity was found, however, within the term group with decelerations. This suggests the presence of two separate study populations, of which one had decelerations, a lower pH and more severe growth retardation (Dijxhoorn et al, 1987), rather than a direct relationship between neurological morbidity and the pH at birth. All eight neurologically abnormal newborn infants of the preterm group had an abnormal FHR pattern which had already been present antepartum in seven of the cases. Four of these eight infants had a more or less normal umbilical artery pH at birth ( > 7.15). In our

120 G. H. A. VISSER

Table 1. Neonatal neurological outcome in relation to antepartum fetal heart rate (FHR) patterns in small-for-dates (SFD) term and preterm fetuses.

Neonatal neurological diagnostic category

pHua NNOS CS (mean) Normal Suspect Abnormal (median)

SFD term fetuses NormalFHR 9 9 7.25 8 1 - - 56 Decelerations 14 14 7.14 3 7 4 51.6 Total 23

SFD preterm fetuses Normal FHR 12 - - 7.18 7 5 - - 53 Decelerative FHR 14 1t 7.16 4 6 4 50.5 Terminal FHR 7 7 6.99 - - 3 4 48.5 Total 33

CS, caesarean section; NNOS, neonatal neurological optimality score; pHua, umbilical artery pH.

Table 2. Outcome in 108 infants born between 25 and 32 weeks with and without signs of intrauterine asphyxia (percentages in parentheses).

Outcome Asphyxia Noasphyxia Pvalue

n 30 78

Gestational age (in weeks: mean + so) 29.8 _ 1.9 29.9 _+ 1.9 Birthweight (in grams: mean+so) 1023+250 1400_+391 <0.05 IUGR 14 4 Caesarean section 28 (93) 40 (51) < 0.05 Apgar score < 7

1 minute 22 (73) 2l (27) <0.05 5 minutes 13 (43) 8 (10) <0~05

Respiratory distress syndrome 21 (70) 49 (63) Severe intraventricular haemorrhage 9 (30) 4 (5) <0.05 Death before 2 years of age 14 (47) 11 (14) <0.05 Neurologically abnormal at 2-5 years 4/16 (25) 8/67 (12)

Modified from Westgren et al (1986).

o p i n i o n these d a t a ind ica te t h a t the o c c u r r e n c e o f a n t e p a r t u m d e c e l e r a t i o n s is m o r e i m p o r t a n t w i th respec t to n e o n a t a l n e u r o l o g i c a l o u t c o m e t h a n the ac tua l p H va lue a t b i r th .

As p a r t o f a f o l l o w - u p s tudy ( H a d d e r s - A l g r a , 1987) all 33 S F D p r e m a t u r e in fan t s were r e - e x a m i n e d a t 4 to 6 years o f age. T w o o u t o f seven w i t h a t e r m i n a l F H R , t w o o u t o f 14 w i t h a dece l e r a t i v e p a t t e r n a n d n o n e o u t o f 12 w i t h a n o r m a l a n t e p a r t u m c a r d i o t o c o g r a m were n e u r o l o g i c a l l y a b n o r m a l ( D i j x h o o r n , 1986).

I n a n o t h e r s tudy 17 I U G R infan ts , de l ive red b e t w e e n 28 a n d 32 w e e k s o f

FETAL HEART RATE PATTERNS AND HANDICAP 121

gestation because of antepartum decelerations, were neurologically examined at 2.5 to 7 years of age (Huisjes et al, 1985). All these infants had been delivered by elective caesarean section. Two were neurologically abnormal: one had a moderate hemiplegia with a normal intelligence; the other was severely handicapped with an asymmetrical spastic diplegia and severe motor retardation, which was associated with congenital adrenal hyperplasia and severe neonatal asphyxia. A third child had a diffuse hypotonia with clumsy motility (minor neurological dysfunction). From these data it was concluded that caesarean section appears acceptable in the management of I U G R with fetal distress in the early part of the third trimester.

Westgren et al (1986) also reported on very premature infants (25 to 32 weeks' gestation). They compared the outcome of 30 infants who had suffered intrauterine asphyxia and 78 who had not. Asphyxia was defined as abnormal antepartum or intrapartum F H R patterns with late decelerations or pro- nounced variable decelerations. Unfortunately no information is given as to how often antepartum F H R abnormalities were present. Their data are summarized in Table 2. In the asphyxia group birthweights and the Apgar scores were lower. Furthermore, the incidence of severe intraventricular haemorrhage and death before the age of 2 years was increased. There were more developmental or neurological abnormalities at 2 years of age in the survivors of the asphyxia group, although the difference with the non- asphyxic infants was not significant.

Lorenz et al (1986) sent a questionnaire regarding neuromotor development of infants to women who had had antepartum F H R abnormalities and to a matched control group. The matching criteria included gestational age, weight at birth and pregnancy complications. In the study group the incidence of F H R abnormalities during labour was increased, as was that of low Apgar scores and of a low umbilical artery pH at birth. The incidence of neuromotor abnormality was more than twice as high (14 as compared to 6 out of 123). In the study group it occurred especially in cases of preterm birth and/or IUGR. Neuromotor abnormalities were, furthermore, related to the degree of antepartum F H R abnormality. These authors advocate an increased use of antepartum F H R monitoring in cases of suspected fetal compromise and a generous use of elective caesarean section. In this study the incidence of caesareans in the study and control group was 44% and 13%, respectively.

In a recent abstract Henderson-Smart et al (1987) presented similar data. Neonatal outcome of 36 preterm infants with an abnormal antepartum F H R pattern, showing recurrent decelerations, was compared with 36 controls matched for gestational age and weight percentiles who were also born to mothers with hypertension, but had a normal F H R pattern. Neonatal neurological development was more often impaired in the group with decelerations, most especially in the subgroup with reduced heart rate variation and shallow decelerations.

DISCUSSION

In all the publications discussed, a relationship between antepartum F H R abnormalities and neurological morbidity was found. This stresses the impact

122 G . H . A . VISSER

of prenatal hypoxaemia on brain development. In IUGR fetuses hypoxaemia is probably associated with chronic hypoglycaemia (Robinson et al, 1985; Soothill et al, 1987) and deprivation of other nutrients. In these fetuses brain damage is more likely to be due to chronic malnutrition (including hypoxaemia) rather than simply to hypoxaemia. This reasoning can to a large extent be supported by the morphological findings in human IUGR infants (Dobbing, 1974) and in animal models (Bedi, 1984) where a smaller brain size, fewer cells, deficits in synapse-to-neurone ratios and reduced dendritic growth are found, rather than distinct, localized lesions. The latter are often founcl after (acute) asphyxia (Kreusser and Volpe, 1984).

These data suggest that growth-retarded fetuses should be delivered before antepartum signs of hypoxaemia occur. Fetuses at risk of developing antepartum heart rate decelerations might be detected by studying velocity waveforms in the umbilical artery as there is increasing evidence that, in IUGR fetuses, changes in these usually precede the occurrence of decele- rations (Reuwer et al, 1987). In 8 of 10 growth-retarded fetuses that we followed longitudinally, abnormal waveforms were present for more than three weeks before decelerations occurred (Visser et al, 1986).

Doppler studies of the fetal aorta also indicate that IUGR fetuses delivered with less severe velocity waveform abnormalities do better than those who lack end-diastolic frequencies (Hackett et al, 1987). This applies to the incidence of mortality, necrotising enterocolitis and haemorrhage.

Delivery before hypoxaemia or severe waveform abnormalities occur implies delivery at an earlier age. During the preterm period this might increase other (neonatal) risks. Only controlled trials can determine a possible beneficial effect. Maternal oxygen administration increases fetal Po2 (Nico- laides et al, 1987) and movements and heart rate variation (Bekedam et al, 1986) in IUGR fetuses. At present it remains uncertain if morbidity can be reduced by this therapy, as it is unlikely that the supply of other nutrients increases as well.

When antepartum late decelerations occur elective (primary) caesarean section seems to be the appropriate mode of delivery, since fetal distress will occur during labour in most of these cases (Visser et al, 1980).

S U M M A R Y

In this paper data on abnormal antepartum FHR patterns are related to the state of fetal oxygenation, fetal brain abnormalities and to neurological outcome. It is concluded that in IUGR fetuses changes in heart rate (and movement) patterns are late signs of impairment. Antepartum heart rate decelerations are usually the first of the abnormalities detected and are associated with fetal hypoxaemia. A fixed or flat F H R pattern might be indicative of congenital malformations of the brain or of prenatally acquired encephalopathy. Several studies have shown that antepartum F H R abnor- malities (usually late decelerations) are associated with an increased risk of subsequent handicap. This risk is related to the degree of F H R abnormality, and especially applies to infants born preterm and/or growth-retarded. Late (ante partum) FHR decelerations seem to be more important than 'asphyxia'

FETAL HEART RATE PATTERNS AND HANDICAP 123

at bir th in de termining (neonatal) neurological outcome. In I U G R hypoxae- mia is p robab ly associated with depr ivat ion of other nutr ients , and thus bra in damage in these infants is more likely to be due to chronic ma lnu t r i t i on ( including hypoxaemia) than to hypoxaemia alone. This reasoning is supported by morphologica l findings in I U G R infants.

In general fetuses should be delivered before an t epa r tum signs of hypoxae- mia appear. Doppler b lood - velocity waveform analyses of fetal vessels may detect fetuses at risk for an t epa r tum decelerations, bu t unt i l now there has been insufficient in fo rmat ion abou t false-positive a b n o r m a l velocity wave- forms to depend absolutely on these. Fur the rmore , delivery at an earlier age may increase the risk of other neona ta l complicat ions.

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