Behavioural state transitions in healthy and growth retarded fetuses

Ear& Human Development, 19 (1989) 155-165 Elsevier Scientific Publishers Ireland Ltd.

155

EHD 00948

Behavioural state transitions in healthy and growth retarded fetuses

Domenico Arduini, Giuseppe Rizzo, Leonardo Caforio, Maria Rita Boccolini, Carlo Romanini” and Salvatore Mancuso

Dept. Obstet. and GynecoL Universit; Cattolich S. Cuore, Roma and “Dept. Obstet. and Gynecol. Universith di Ancona (Italy)

Accepted for publication 5 August 1988

Summary

The transitions, i.e. time intervals between two different behavioural states, were studied in 10 healthy and 10 growth retarded fetuses (IUGR) in near term pregnancies. In healthy fetuses, transitions usually lasted less than 3 min whereas IUGR fetuses showed a longer duration when compared to healthy fetuses. Moreover, a significant trend in the change of state variables (fetal heart rate, fetal eye movements and fetal gross body movements) was evident in healthy fetuses: fetal heart rate was the first variable to change in transitions from IF to 2F and the last variable to change in transitions from 2F to 1F. On the other hand IUGR fetuses showed a random sequence in order of change. These findings were substantiated by the intra- individual consistency evidenced in repeated recordings. In conclusion the analysis of transitions differentiates between healthy fetuses and those affected by IUGR.

behavioural states; transitions; fetal growth retardation.

Introduction

In the past few years non-invasive technologies, by enhancing the possibility of observing the human fetus in utero, have generated an increased interest in the potential assessment of fetal functional development. Several activities such as fetal heart rate (FHR) [l 11, gross body movements (FM) [6], eye movements (FEM) [7]

Correspondence to: Dr. Domenico Arduini, 1st. Cl. Ostetrica e Ginecologica, Universith Cattolica S. Cuore, Largo A. Gemelli, 8.00168 Roma, Italy.

0378-3782/89/$03.50 0 1989 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland

156

and breathing movements (FBM) 115) have been investigated in order to monitor fetal well-being, but the low predictive value of the separate assessment of these parameters obtained in quantitative analysis limits their significance in clinical prac- tice.

Nijhuis et al. [14] first evidenced stable and recurring associations between FHR, FEM and FM similar to those used by Prechtl [16] for the identification of behavioural states in the newborn. These associations become particularly evident after 36 weeks of gestation thus permitting the identification of four different behavioural states (1F to 4F) in the human fetus. Several authors [4,13,23] have reported delays in the developmental course of behavioural states in compromised fetuses. How- ever, the long observation period (i.e. 2 h) required for behavioural state analysis has to date limited their clinical application.

The aim of this investigation was to assess whether the isolated analysis of transitions, i.e. time intervals between two different and consecutive behavioural states [14], can differentiate between healthy fetuses and fetuses affected by intrauterine growth retardation (IUGR) characterized by abnormal blood flow velocity waveforms.

Subjects and Methods

After informed consent was obtained, 10 healthy pregnant women and 10 women with pregnancies complicated by fetal growth retardation were admitted to the study. All these women were nulliparae with a reliable gestational age as assessed by certainty about last menstrual period and early second trimester ultrasonographic examination. In order to standardize the population of IUGR fetuses we selected only fetuses who fulfilled the following criteria: ?? ultrasound measurement of abdominal circumference below the 10th centile of

the curves of Campbell and Wilkin [8]

TABLE I

Clinical features of healthy fetuses.

No. of fetus

Sex Gestational Gestational age at age at recording delivery

Birthweight (g) (centile)

Apgar score Umbilical (1 min--5 min) artery pH

1 F 36 + 1 2 F 36 + 4 3 M 31 + 2 4 F 36 + 6 5 M 37 + 4 6 M 36 + 5 I M 31 + 1 8 F 36 + 3 9 M 31 + 0

lo” F 36 + 4

40+2 39 + 5 40 + 5 41 + 0 38 + 5 40+4 39 + 5 40+4 41 + 2 39 + 4

3230 (25-50) 2890 (10-25) 3420 (50-75) 3610 (50-75) 3280 (25-50) 3980 (75-90) 3050 (50-75) 3750 (50-75) 3160 (25-50) 3480 (50-75)

9-10 7.32 9-9 - 8-10 7.29

10-10 1.33 8-9 - 9-10 1.34 8-10 7.30 8-10 - 9-10 - 7-9 1.27

‘Breech presentation.

157

?? abnormal fetal blood flow velocity waveforms as expressed by a ratio between the pulsatility indexes of umbilical artery and internal carotid artery above the first standard deviation of our reference range [3]

?? absence of fetal malformations, chromosomal aberrations or intrauterine infec- tions

?? normal cardiotocograms (i.e. baseline varying between 120 and 160 beats/min, presence of periodic accelerations and absence of decelerations) at the time behavioural studies were performed

?? absence of maternal medications except iron and folate supplementations ?? postnatal confirmation by a birthweight below the 10th centile for Italian popula-

tion standards [12]

The overall characteristics of the two groups of patients are summarized in Tables I and II. All fetuses in the control group were vaginally delivered except in one case in which a cesarean section was performed for a breech presentation. The outcome confirmed the good health of the fetuses studied.

In three patients with IUGR fetuses a mild hypertension without proteinuria was detected. Two patients were smokers (7 and 10 cigarettes/day, respectively) whereas the remaining cases showed no obvious causes for growth retardation. All IUGR fetuses were delivered by cesarean section. The primary indications for cesarean section were fetal distress (i.e. abnormal heart rate tracings) in eight cases and breech presentation and cervical dystocia in the remaining two cases.

In both groups behavioural studies were carried out at a gestational age between 36 and 38 weeks, in the afternoon, 2 h after a 1500 kcal standardized lunch. Record- ings were performed in a quiet room on patients lying in a comfortable semi-recum- bent position according to a technique reported elsewhere [2]. Briefly, FHR, FM and FEM were simultaneously recorded for two consecutive hours. FHR was obtained by means of a Hewlett Packard 8040 cardiotocograph equipped with an external ultrasound transducer and stored on-line into a Digital PDP 11 computer [19]. FEM and FM were determined by two observers using two real-time ultrasound machines (Ansaldo AUC 940 and Ansaldo Esacord 80) positioned to obtain a parasagittal section through the fetal face and a transverse section at the level of the upper fetal abdomen, respectively.

The two observers entered individual movements into the computerized system using two remote switching devices and pushing codified keyboards from onset to end of each movement. Similarly, the observers entered the failure periods in which a reliable view of the fetal lens or trunk was not obtained. Observers were not allowed to see the FHR tracing or to hear the heart-beat sound. The quality of the FHR tracing was checked by a third operator.

At the end of the recordings polygraphic printouts of the variables (FHR, FEM and FM) were automatically provided and were labeled by random numbers and analysed later. Investigators involved in the subsequent analysis were not informed of the sequence of numbers used.

The off-line analysis of computer printouts was performed as follows. First FHR was classified into four different patterns (i.e. A,B,C,D) using a 3-min moving window as described by Nijhuis et al. [12]. FEM and FM classified as present or absent

TAB

LE I

I

Clin

ical

fea

ture

s of

gro

wth

-ret

arde

d fe

tuse

s.

No.

of

fetu

s

1 2 3 4 5 6 7 8 9 10

Sex

M

F F M

M

F F F M

M

Ges

tatio

nal

age

Ges

tatio

nal

age

Birt

hwei

ght

Apg

ar s

core

U

mbi

lical

at

rec

ordi

ng

at d

eliv

ery

(g) (

cent

ile)

(1 m

in -

5 m

in)

arte

ry P

H

36 +

3

31 +

4

2150

(5-1

0)

8-9

1.23

36 +

2

38 +

0

2430

(5-1

0)

l-9

7.27

36

+ 4

31

+ 5

20

80 (2

.3-5

) 5-

8 7.

19

36 +

2

39 +

1

2530

(5-1

0)

8-10

1.

26

37 +

2

37 +

6

1950

(< 2

.3)

6-8

7.20

37 +

5

38 +

6

2430

(5-1

0)

8-9

1.24

37 +

3

38 +

4

2390

(5-1

0)

7-9

-

37 +

1

39 +

3

2480

(5-1

0)

7-8

7.22

36 +

4

37 +

5

2135

(2.3

-5)

6-8

1.26

36 +

3

37 +

2

2610

(5-1

0)

8-8

7.21

Rem

arks

Mild

hyp

erte

nsio

n,

late

dec

eler

atio

ns,

plac

enta

l in

farc

ts

Red

uced

FH

R v

aria

bilit

y M

othe

r sm

okin

g 7

ciga

rette

s/da

y la

te d

ecel

erat

ions

, pl

acen

tal

infa

rcts

V

aria

ble

dece

lera

tions

La

te d

ecel

erat

ions

, pl

acen

tal

infa

rcts

M

ild h

yper

tens

ion,

br

eech

pre

sent

atio

n,

plac

enta

l in

farc

ts

Mild

hyp

erte

nsio

n,

redu

ced

FHR

var

iabi

lity,

va

riabl

e de

cele

ratio

ns

Mot

her

smok

ing

10 ci

gare

ttes/

day,

va

riabl

e de

cele

ratio

ns

Rup

ture

of

mem

bran

es,

cerv

ical

dys

toci

a V

aria

ble

dece

lera

tions

159

1 2 3 4 5 6 7 8 min

F H c” R 6

A !

F + M _ J

F ??E

- tl b :t b: 4 Coi ncilence 1 F Transitional period Coincidence 2F

1F - 2F

Fig. 1. Profile of state variables during a 1F to 2F transition in a healthy fetus.

were analysed using the same 3-min moving window technique. The temporal pro- files so obtained from the three variables (FHR, FEM and FM) were then combined for the analysis of behavioural states and transitional periods (Fig. 1). When the state variables fulfilled one of the specific combinations described by Nijhuis et al. [14], periods were classified as “coincidence” (1F to 4F). Transitions were considered as the time intervals elapsing between two different and stable periods (greater than 3 min) of coincidence. In this investigation we calculated the duration of transitions and the sequence of change of behavioural variables during this time interval.

In order to evaluate the degree of intra-individual variations all fetuses were studied for two consecutive days with the same technique. Data are given as medians, lower (Ql) and upper (43) quartiles and ranges. Statistical analysis was performed by means of Mann-Whitney U test and chi-square test.

Results

The percentage distribution of periods of coincidence in both groups are reported in Table III. The incidence of periods of no coincidence was increased (P< 0.001) in IUGR fetuses as compared to healthy fetuses. However, the coincidence 1F was lower (P < 0.02) in the IUGR fetuses than in the healthy fetuses. No difference was found for coincidences 2F, 3F and 4F. When the results obtained on the two consecutive days of recording were compared, no statistical differences were found within the two groups.

The incidence of periods of coincidence 3F and 4F was too low to allow a reliable assessment of transitions between these periods. The analysis of transitions was therefore restricted to the periods from 1F to 2F and 2F to IF. The number and duration of transitions are given in Table IV. IUGR fetuses showed a longer duration of transitions when compared to healthy fetuses in both 1F to 2F and 2F to 1F transitions. However, no differences were found within each of the two groups when the two repeated recordings were considered.

Concerning the sequence of change of behavioural variables during the transitions from 1F to 2F (Table Va), FHR was the first variable to change (from FHR pattern A to FHR pattern B) in healthy fetuses, whereas in IUGR fetuses no signifi-

160

TABLE III

Distribution of the percentage of coincidence and no coincidence in the two groups of fetuses studied for each day of recording.

Healthy fetuses IUGR fetuses

1st day 2nd day 1st day 2nd day

Coincidence 1F Median Ql-Q3’ Range

Coincidence 2F Median Ql--43 Range



No coincidence Median Ql--43 Range

28.5 21.5 17* 15’ 16-34 15-22 12-22 7-21 9-40 l-32 o-31 o-34

54.5 53 45 49 48-60 39-64 36-50 42-62

2 values 1 value 2 values 1 value 396 3 2,8 6

2 3 o-5 o-9 O-32 O-50

14.5 15.5 34** 29** 11-24 l-22 20-45 23-38 8-32 5-30 10-46 8-47

3 values 2 values 8,32,24 25,9

a Ql = lower quartile; 43 = upper quartile. Statistical analysis was performed by means of Mann-Whitney U-test. *P ( 0.02; **P < 0.001 vs. healthy fetuses.

TABLE IV

Duration(s) of transitions in the two groups of fetuses studied for each day of recording.

Healthy fetuses IUGR fetuses

1st day 2nd day 1st day 2nd day

Transitions lF-2F No. 16 18 10 11 Median 130 140 290** 280** Ql--43 70-160 95-180 210-440 105-390 Range 40-250 50-300 60-600 70-500

Transitions 2F--1F No. Median Ql--43 Range

20 22 23 19 125 150 310** 300** 95-155 80-180 180-410 190-395 50-350 40-360 100-480 90-700

Statistical analysis was performed by means of Mann-Whitney &test. ??*P< 0.001 vs. healthy fetuses.

TAB

LE V

a

Tem

pora

l se

quen

ce o

f th

e ch

ange

s of

beh

avio

ural

va

riabl

es,

i.e.

FHR

. FE

M a

nd F

M d

urin

g tra

nsiti

ons

from

1F

to 2

F in

the

two

grou

ps o

f fe

tuse

s st

udie

d fo

r ea

ch d

ay o

f re

cord

ing.

Hea

lthy

fetu

ses

(%a)

1st d

ay

FHR

FE

M

FM

2nd

day

FHR

FE

M

FM

IUG

R f

etus

es (

%)

1 st d

ay

FHR

FE

M

FM

2nd

day

FHR

FE

M

FM

1st v

aria

ble

to c

hang

e 2n

d va

riabl

e to

cha

nge

3rd

varia

ble

to c

hang

e Si

gnifi

canc

e (P

)”

FHR

vs.

FEM

FH

R v

s. FM

FE

M v

s. FM

12/1

6 l/1

6 (7

5)

(6)

3/16

7/

16

(19)

(4

4)

l/16

8/16

(6

) (5

0)

GO

.001

<O

.ool

n.

s.

3/16

15

118

2/18

(1

9)

(83)

(1

1)

6116

2/

18

7/18

(3

7)

(11)

(4

0)

7/16

l/l

8 9/

18

(44)

(6

) (4

9)

<O.o

ol

~0.0

01

n.s.

l/18

4110

3/

10

3/10

5/

11

3111

3/

11

(6)

W)

(30)

(3

0)

(46)

(2

7)

(27)

9/

18

2/10

4/

10

4/10

4/

11

5/11

2/

11

(49)

(2

0)

W)

(40)

(3

6)

(46)

(1

8)

818

4/10

3/

10

3/10

2/

11

3/11

6/

11

(45)

(4

0)

(30)

(3

0)

(18)

(2

7)

(55)

n.s.

n.s.

n.s.

n.s.

n.s.

n.s.

‘Sta

tistic

al a

naly

sis

was

per

form

ed

by m

eans

of

x2-te

st.

TAB

LE V

b

Tem

pora

l se

quen

ce o

f th

e ch

ange

s of

beh

avio

ural

va

riabl

es,

i.e.

FHR

, FE

M a

nd F

M d

urin

g tra

nsiti

on

perio

ds f

rom

2F

to 1

F in

the

two

grou

ps o

f fe

tuse

s st

ud-

ied

for

each

day

of

reco

rdin

g.

Hea

lthy

fetu

ses

(Vo)

1 st d

ay

FHR

FE

M

FM

2nd

day

FHR

FE

M

FM

IUG

R f

etus

es (

o/o)

1st d

ay

FHR

FE

M

FM

2nd

day

FHR

FE

M

FM

1st v

aria

ble

to c

hang

e 2n

d va

riabl

e to

cha

nge

3rd

varia

ble

to c

hang

e Si

gnifi

canc

e (P

Y

FHR

vs.

FEM

FH

R v

s. FM

FE

M v

s. FM

2/20

8/

20

10/2

0 4/

22

7/22

(1

0)

(40)

(5

0)

(18)

(3

2)

3/20

10

/20

7/20

2/

22

1312

2 (1

5)

(50)

(3

5)

(9)

(49)

15

/20

2/20

3/

20

16/2

2 2/

22

(75)

(1

0)

(15)

(6

3)

(9)

<O.O

Ol

<O.o

Ol

n.s.

<O.O

Ol

<O.o

Ol

n.s.

II/2

2 91

23

8/23

(5

0)

(40)

(3

4)

7122

7/

23

9/23

(3

2)

(30)

(4

0)

4/22

71

’23

6/23

(1

8)

(30)

(2

6)

n.s.

ll.S.

n.s.

6/23

61

19

8/19

5/

19

(26)

(3

1)

(43)

(2

6)

7/23

8/

19

4/19

7/

19

(30)

(4

3)

(20)

(3

7)

IO/2

3 5/

19

7/19

71

19

(44)

(2

6)

(37)

(3

7)

n.s.

n.s.

n.s.

%at

istic

al

anal

ysis

was

per

form

ed

by m

eans

of

x3-te

st.

163

cant trends were found. In contrast, in healthy fetuses FHR was the last variable to change during the transitions from state 2F into 1F (Table Vb), whereas no significant trend was found indicating that FM or FEM was the first variable to change. Furthermore, IUGR fetuses showed a random sequence in the order of change. No statistical differences were found between the two repeated recordings.

Discussion

In the present investigation we studied a group of fetuses affected by growth retardation characterized by abnormal blood flow velocity waveforms at Doppler ultrasound examination. These fetuses present haemodynamic changes characterized by a redistribution of cardiac output with an increased perfusion to the brain and a decreased blood flow to peripheral districts. Notwithstanding the presence of this condition of relative “brain sparing” [lo], the normal development of fetal behaviour is impaired in this condition, as recently found by Bekedam et al. [5] and Van Vliet et al. [23]. Furthermore, these behavioural modifications seem to be related to the severity of the haemodynamic changes (181. The causes of this impaired development are still unknown; it can be speculated that the chronic hypoxia and nutrient limitations usually present in these fetuses may play an impor- tant role in determining behavioural abnormalities.

In agreement with these data, the IUGR fetuses in this study had an increased number of periods of no coincidence and a decreased coincidence lF, if compared with healthy fetuses. The marked abnormalities found in IUGR fetuses suggest a higher level of compromise in the IUGR fetuses studied when compared to IUGR fetuses of other reports [23].

In the healthy fetuses of the control group, transitions usually last less than 3 min. This condition of relative simultaneity of the changes of state variable, together with their stable coincidence, allows to identify in these fetuses “true behavioural states” as described by Prechtl [17]. On the other hand, all the IUGR fetuses studied showed longer transitions with respect to healthy fetuses and these differences were evident during both transitions from 2F into IF and from 1F into 2F. It was therefore impossible to identify true behavioural states in these IUGR fetuses and only coincidence of behavioural variable could be detected.

The sequence of change of behavioural variables during transitions must be pointed out. In healthy fetuses, FHR showed a significant preference to be the first variable to change during transitional periods IF to 2F, whilst it was the last variable to change during 2F to 1F transitions.

These particular sequences, recently reported also by Swarties et al. [22] by means of a different technique of analysis, differ from the findings obtained in the newborn by Shirataki and Prechtl [20], who found no leading state variable during transitions.

This discrepancy could be explained by the different mechanisms regulating the alternation of behavioural states during intrauterine life with respect to the neonatal period. Fetal behaviour exhibits circadian rhythms that are immediately lost at birth [9,21]. Although the mechanism regulating the alternation of behavioural states is

164

still obscure, several findings suggest a possible maternal hormonal influence [ 11. We previously reported in healthy fetuses that the maternal administration of naloxone results in the modification of behavioural states with a change from state 1F into 2F or 4F [2]. Of interest is that FHR was the first variable to change in all the cases treated with naloxone (unpublished data), suggesting that the mechanism involved in the alternation of behavioural states in the human fetus could first act on the regulation of FHR during the changes from state 1F into 2F or 4F. Similarly, it can be speculated that during the transitions from state 2F into lF, FHR should be the last variable to be changed. The loss of maternal influences after birth could modify the mechanism regulating the alternation of behavioural studies and this different situation could explain the absence after birth of a preferential sequence of change of behavioural variables during transitions.

IUGR fetuses, however, did not show this particular sequence of state variables during transitions. This condition, associated with the long duration of transitions, suggests that in these fetuses the regulation of the alternation of behavioural states has not attained the same level of organization, and synchronization, shown by healthy fetuses.

Finally, the adequate reproducibility assured by the intra-individual consistency evidenced in repeated recordings, together with the relative technical simplicity of this analysis might allow its application in the future to monitor fetal functional development. Further studies are required on a larger number of low and high risk fetuses in order to clarify the developmental course of transitions and to confirm their alterations in compromised fetuses. Such studies are in progress.

References

1

2

3

4

5

6

7

8

9

10

Arduini, D., Rixzo, G., Parlati, E., Giorlandino, C., Valensise, H., Dell’Acqua, S. and Romanini, C. (1986): Modifications of &radian and circadian rhythms of fetal heart rate after fetal-maternal adrenal gland suppression: a double blind study. Prenat. Diagn., 6,409-417. Arduini, D., Rizxo, G., Dell’Acqua, S., Mancuso, S. and Romanini, C. (1987): Effect of naloxone on fetal behaviour near term. Am. J. Obstet. Gynecol., 156,474-478. Arduini, D., Rizzo, G., Romanini, C. and Mancuso, S. (1987): Fetal blood flow velocity waveforms as predictors of growth retardation. Obstet. Gynecol., 7,7-10. Arduini, D., Rixzo, G., Caforio, L. and Mancuso, S. (1987): Longitudinaldevelopment of behavioural statesinhydrocephahcfetuses. FetalTherapy,Z, 135-143. Bekedam, D.J., Visser, G.H.A., de Vries, J.J. and Prechtl, H.F.R. (1985): Motor behaviour in the growth retarded fetus. Early Hum. Dev., 12, 155-165. Birnholz, J.C., Stephens, J.C. and Faria, M. (1978): Fetal movement patterns: a possible mean of defining neurologial milestones in utero. Am. J. Roentgenol., 130,537-540. Bots, R.S.G.M., Nijhuis, J.G., Martin, C.B. Jr. and Prechtl, H.F.R. (1981): Human fetal eye movements: detection in utero by means of ultrasonography. Early Hum. Dev., 5,87-94. Campbell, S. and Wilkin, D. (1975): Ultrasound measurement of fetal abdomen circumference in estimationof fetalweight. Br. J.Obstet. Gynaecol., 82,680-689. Dawes, G.S. (1986): The central nervous control of fetal behaviour. Eur. J. Obstet. Gynecol. Reprod. Biol., 21.341-346. Eyckvan,J.,Wladimiroff,J.W.,Noordam,M.J.,vandenWijngaard,J.A.G.W.andPrechtl,H.F.R. (1988): The blood flow velocity waveforms in the fetal internal carotid and umbilical artery; its relationship to fetal behavioural states in the growth retarded fetus at 37-38 weeks of gestation. Br. J. Obstet,Gynaecol., 95,437-447.

165

11

12

13

14

15

16

17

18

19

20

21

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Behavioural state transitions in healthy and growth retarded fetuses

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