Fetal respiratory movements: Relationship to postnatal respiratory capacity STEEN :-.JELDAM, M.D. Copenhagen, Denmark Sixty-six normal and 346 pathologic pregnancies have been investigated by means of dynamic ultrasound for determination of fetal intrauterine respiratory amplitudes in over 930 scans of 30-minute duration. Ten fetuses developed respiratory distress syndrome (ROS), and all of these showed antenatally either falling (more than 2 SO) or abnormally low thoracic and abdominal amplitudes. No fetuses with amplitude measurements within the normal range (mean:+: 2 SO) developed RDS (p < 0.001, x2 test). In 74 women, measurement of amniotic lecithin was performed within one half hour before a dynamic ultrasound registration of the thoracic and abdominal amplitudes. No significant difference was found in sensitivity, predictive value, or specificity between these two methods in identifying ROS. The conclusion is that the pathogenesis of ADS may be both biochemical and biophysical, and that this new noninvasive method may easily be used as a screening test for postnatal respiratory capacity in high-risk pregnancies, since only 10 equal and regular respiratory movements are needed for this measurement. (AM. J. OssTET. GYNECOL. 142:862, 1982.)
fetal respiratory movements m utero was suggested by Ahlfeld 1 in 1905, but 65 years passed before Dawes and associates 2 showed that respiratory movements really existed by making continuous direct measurements of pressure from catheters chronicallv implanted in the fetal lamb trachea. When Boddy and associates,:3 in 197 4, found that the fetal lamb responded to hypoxia with a diminution of fetal breathing movements and gasping, they used ultrasound A-mode as a noninvasive method to measure movements of the human fetal chest wall in order to examine whether their observations in the lamb were true also for the human fetus. In 1975, they published 4 observations on 200 antenatal patients after the thirtysixth week. and they found that, in 10 of 11 fetuses shortly before intrauterine death, normal breathing was absent and that gasping movements appeared 24 to THE PRESENCE OF
From the Department of Obstetrics and Gynecology YB, Depmtment of Diagnostic Ultrasound Y, Rigshospitalet, University Hospital. Reaivedjor publication july 27, 1981. Aaepted November 2, 1981.
Reprint reques~1.· Steen Neldam, M.D., Department of Obstetrics and Gynecology YB, Rigshospitalet 4021, Blegdarnsvej 9, DK-2100, Copenhagen, Denmark.
862
72 hours before intrauterine death. On the other hand, the continued presence of normal fetal breathing movements (FBM) was found to be a useful indicator of good health. These first results were almost "too good to be true," as Boddv himself stated.' But since his publication. most work on FBM has dealt with the possibility of assessing the degree of fetal asphvxia and of predicting fetal distress in labor and fetal outcome, according to the presence or absence of fetal respiratory movements (FRM).:;-r In spite of intensive research, these original promising results have not yet pro\·ided the answer to the difficult problems (for instance, timing of delivery) of high-risk pregnancies that they were expected to solve.H The aim of this study was to determine whether a relationship exists between intrauterine FRM and postnatal respiratory capacity of the child, as proposed in our preliminary report. 9
Material. •nd methods Sixty-six normal and 346 pathologic pregnancies were investigated by means of dynamic ultrasound for determination of FBM in over 930 scans. The equipment consisted of an Aloka SSD-202 Echo Camera, a linear-array scanner with a 64 element probe, modified with a select-line facility. Via a select-line knob a certain 0002-9~~7R/R2/070R62+05$00.50/0
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1982 lh<- C. \' \losbv Co
Volume 142 :>Jumber 7
Fetal respiratory movements: Postnatal capacity
863
T4mm.
Fig. l. Fetal respiratory amplitude measurements at the thirty-sixth gestational week. The mother had diabetes mellitus (White. Class D). T =thoracic; A = abdominal amplitude.
element in the transducer could be selected, and the received and amplified signal from this element (Mmode) was taken out to a Honeywell LS-6B fiber optic recorder. This meant that all movements under this line could be recorded on the light-sensitive paper on the Honeywell recorder. Fig. 1 shows such a recording. The scanning of the fetal thoracic and abdominal wall movements was performed as a longitudinal scan in the median plane, and the selected line was placed on the middle of the sternum and just beneath the diaphragm. The amplitude of the thoracic and abdominal movements could then be measured directly on the paper, as seen in Fig. 1. Most of the scans were performed before noon, and lasted 30 minutes . The measurements were done on at least 10 equal, regular respirations. The clinicians were not aware of the results of the FBM registration. The respiratory amplitudes of these 412 fetuses were compared with those in our normal material, 10 which consisted of ;)5 uncomplicated pregnancies, all of which eventuated in healthy children without postnatal respiratory problems (see Fig. 2). The respiratory distress syndrome (RDS) was defined 11 as: ( l) the presence of at least two of the following four clinical symptomstachypnea (frequency more than 60 beats/min), grunting , retractions, and cyanosis on exposure to atmo-
spheric air: (2) lungs showing a diffuse. small-dotted reticulogranular pattern on pneumobronchoradiography ; and/or (3) the presence of pulmonary atelectasis and hyaline membranes on autopsy. Only in women with diabetes was amniotic lecithin measured routinely ~n the thirty-fifth week. Results
Of the 412 fetuses investigated. I 0 developed RDS, and one of these infants died at 24 hours of age (weight, I ,910 gm). In all of these cases, antenatally, there was either abnormally low thoracic and abdominal amplitudes or decreasing amplitudes (more than 2 SD). ln 74 women, amniotic lecithin was measured within one-half hour before registration by dynamic ultrasound of the thoracic and abdominal respiratory amplitudes . In the group of infants with RDS, the amniotic lecithin was normal in five cases, abnormally low in one (below 40 1-1-mol/L), and not measured in the other four (Table 1). An example of the decline in respiratory amplitude is seen in Fig. 2, where the thoracic and abdominal amplitudes of the fetus of Patient 4 (Table I) are compared to the Yalues for the normal material. The remainder of the fetus (n = 402) had no postnatal respiratory problems. Three of these 402 patients had an abnormally low amniotic health value 8 or
864
Neldam Am.
THORACAL AMPLITUDE mm
NORMAL N"'35
5 4
r= 0,973 p<0,001
3
f,~~
2
ABDOMINAL AMPLITUDE mm
N~AL
N=35
5 r=0,920 p<0,001 COJ\FIDENCE LIMITS :t2SD
4
3 2
,...,...--.--.,.--..----,-......,.--.WEEKS OF GESTATION 20 24 2S 32 36 40
Fig. 2. Thoracic and abdominal respiratory amplitudes of the
fews of Patient 4 (Table I) compared to normal values.
9 days before delivery, and also when the measurement was repeated one week later. These patients had normal respiratory amplitudes on dynamic ultrasound measurement and did not develop RDS. As seen in Table II, there is no significant difference between the lecithin and respiratory amplitudes in predicting RDS (Fisher test), although the measurements of amplitude tend to have a higher sensitivity. predictive value, and specificity. However, low amplitude or an amplitude decreasing more than 2 SD identified significantly better the infants with RDS than when the amplitudes were within the normal range (p < 0.001, X2 test).
Comment The value of the lecithin/sphingomyelin (LIS) ratio or the measurements oflecithin in amniotic fluid is well known. The false positive rate is very low. The false negative rate is reported to be 2.6% in a general population, 12 whereas in diabetic pregnancies it has been reported to be between 3% 13 and 18%. 14 Low gestational
J.
:\pril l, 198~ ObsteL Cvnecol
age, fetal asphyxia, and maternal diaberes melhtu~ are the factors most commonly associated \'.ith RDS,"' and Roberts and associates 16 showed in their studv. which was corrected for gestational age and route of deliver~. that RDS is five times more likely to occur in infanb of mothers with diabetes mellitus than in other infants. Therefore, it is very important in diabetic pregnancies to make certain that the fetal lungs are mature before delivery, which is often induced 3 weeks before term. Very promising is the finding that there seems to be a relationship between this noninvasive intrauterine rm:asuring of the respiratory amplitudes and the occurrence of RDS (p < 0.001, x2 test). The practical consequences ofthis study are several. ( 1) Late amniocentesis with determination of lecithin in diabetic and other high-risk pregnancies could be avoided in most case,, and performed only when the amplitude mea,urements are either unsatisfactory or abnormal km. (2) Fetuses with an abnormally low intrauterine respiratory amplitude could be treated immediately postnatallv with oxygen or nasal continuous positive air\\·;n pressure (CPAP) for 24 hours to prewm the full development of RDS. (3) A low lecithin value might abo indicate treatment of the mother with betamethasone 17 if the amplitude measurements are pathologic. However, these considerations need further investigation. The relationship between diminished intrauterine respiratory amplitude and RDS seems to be obscure. The lack of correlation between fetal weight and respiratory amplitude, but positive correlation to gestational age and postnatal respiratory capacity .11 ' seems to indicate that the size and shape of the amplitude depend on the neuromuscular development of the respirator\ muscles and the compliance of the lungs and thoracic cage. The movements of the t boracic wall could in some wav ~timulate the production ot' lecithin or the outfiow of lecithin-containing amnioti( Huid from the lungs. Finallv, could weak intrautennc respiratorv mm ements be a warning that respiratorv mo,·cments postnatallv will be too inadequate to expand the lungs sufficiently? In conclusion, it seems probable, on the basis of the above-mentioned measurements, that the pathogenesis of RDS might be both biochemical and biophysicaL The observation of fetal breathing amplitude by means of dynamic ultrasound scanning could be used to screen for the postnatal respiratory capacitv of the fetus in high-risk pregnancies. The test is easily performed, since only l 0 equal and regular respiratory movements are needed for the registration. An abnormal result of this noninvasive method should be checked with measurements of lecithin in amniotic Huid. The clinical use
Fetal respiratory movements: Postnatal capacity
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Table I. Data on infants developing RDS Condition of infant Patient No.
2 3 4 5 6 7 8 9* 10
Clinical condition of mother
Intrauterine growth retardation, low E 3 + human placental lactogen Diabetes mellitus (Class F) preeciampsia Preterm labor Two stillbirths Diabetes mellitus (Class D) Preeclampsia Pretenn rupture of membranes Preeclampsia Rhesus immunization Diabetes mellitus (Class D)
Amniotic lecithin ( 11-mol/L)
FBM (%)
Respiratory amplitude
Apgar score
Iarterial Umbilical IWeight pH
130
46.1
Falling 2 SD
8110
2,430
Acute cesarean section
40
21.0
Falling 2 SD
9/10
7.20
1,600
Elective cesarean section
90.0 92.0 17.0 0
Falling 2 SD Falling 2 SD Falling 2 SD Pathologically low Falling 2 SD
8/9 7110 5/9 5110
7.26 7.20 7.33
2,450 2,700 2,580 1,410
Elective cesarean section Elective cesarean section Elective cesarean section Acute cesarean section
8/10
7.36
1,910
Falling 2 SD Falling 2 SD Pathologically low
7/10 9/10 6/9
7.24
2,700 2,585 3,180
Spontaneous, died at age 28 hr Elective cesarean section Vaginally Elective cesarean section
130
16.7 130 70, 40, 20 40
23.3 6.5 98.0
Delivery
(gm)
*Weekly amniotic lecithin measurements were performed because of rhesus immunization.
Table II. Evaluation of amniotic lecithin and respiratory amplitude measurements in assessing RDS Sensitivity (TP!TP + FN) F eia/ diagnostic resr
Amniotic lecithin Respiraiory ampliiuue Fisher test Respiratory amplitude of total material
No.
I
I
1/6 6/6
Predictive value (TPITP + FP)
%
No.
16
1/3 6/6
100
p = NS 10110
I
I
Specificity (TNIFP +TN)
%
No.
33 100
73/75 73/73
100
402/402
p = NS 100
10/10
I
I
% 97.3 100
p = NS 100
TP = True positive; FN = false negative; FP = false positive; TN = true negative. of a pathologic result of this new test, together with postponement of the delivery, prophylactic postnatal administration of oxygen, and CPAP, to prevent RDS
I would like to express my gratitude to Arne ~reo sen, M.Sc.E.E., medical technical department, Rigshospitalet, for his modifications of the equipment.
and even lesser respiratory problems (as i.e., apnea and tachypnea) needs further investigation.
REFERENCES I. Ahlfeld, F.: Die intrauterine Tatigkeit der Thorax- und Zwerchfellmuskulatur. Intrauterine Atmung, Monatsschr. Geburtshilfe Gvnaekol. 21:143, 1905. 2. Dawes, G. S., F~x. H. E., Leduc, B. M., and Liggens, G. C.: Respiratory movements and paradoxial sleep in the feoeral iamb,J Physiol. (Lond.) 2i0, 47, 1970. 3. Boddy, K., Dawes, G. S., Fisher, R., Pinter, S., and Robinson, J. 5.: Foetal respiratory movements, electrocortical and cardiovascular responses to hypoxaemia and hypercapnia in sleep, J. Physiol. (Lond.) 243:599, 1974. 4. Boddy, K., and Dawes, G. S.: Fetal breathing, Br. Med. Bull. 31:3, 1975. 5. Platt, L. D., Manning, F. A., Lemay, M., and Sipos, L.: Human fetal breathing: Rt;lationship to fetal condition, AM. j. 0BSTET. GYNECOL. 132:514, 1978. 6. Trudinger, B.J., Gordon, Y. B., Grudzinskas,J. G., Hull, M.G. R., Lewis, P. J., and Arrans, M. E. L.: Fetal breath-
ing movements and other test of fetal well-beii-lg. A comparative evaluation, Br. Med. J. 2:577, 1979. 7. tvfanning. F. A., Platt, L. D., and Sipos, L.: Antepartum
8. 9.
10. I l.
fetal evaluation: Development of a fetal biophysical profile, AM.J. 0BSTET. GYNECOL. 136:787, 1980. Lewis, P., and Boyian, P.: Fetal breathing: A review, AM. j. 0BSTET. GYNECOL. 134:587, 1979. Neldam, S.: Fetal body and respiratory movements, in Kurjak, A., and Rippmann, E. T., and Sulovic, V., editors: Current Status of EPH Gestosis, International Congress Series No. 534, Amsterdam, Excerpta Medica, pp. 224-229. Neldam, S.: Fetal respirarory movements: A nomogram for fetal thoracic and abdominal respiratory movements. Submitted for publication. Osler, M., Faero, F., Hansen, B., and Trolle, D.: Prevention of the respiratory distress syndrome (RDS) by an-
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April i,
Neldam Am.
tepartum glucocorticoid (betamethason) therapy com· bined with phenobarbitone and ritodrine, Dan. Med. Bull. 25:225, !97R. 12. Donald . .J. R., Freeman, R. K., Goebelsmann, U., Chan, W. H .. and Nakamura, R. M.: Clinical experience with the amniotic fluid lecithin/sphingomyelin ratio, AM. J. 0BSTET. CYNECO!.. 115:54i, 19i3. U. Gabhe, S., Lowensohn, R., Mestman.J., Freeman, R., and ( ;oebelsmann, l' .: The lecithin/sphingomyelin ratio in pregnancies complicated by diabetes mellitus. AM. J. 0BSTET GYNECOL. 128:757. 1977. H. \lueller-Heubach, E .. Caritis. S. !'\., Edelstone. D. I., and Tttrner, J. E.: Lecithin/sphingomyelin ratio in amniotic lluid and its \'alue for prediction of neonatal respiratory
l9H~
I Obstel. (;vnecol.
distress syndrome in pregnant diabetic women, AM. J. 0BSTET. CYNECOL. 130:28, 1978. l.'i. Strang. L. B.: Neonatal respiration. Physiological and clinical studies. Hyaline membrane disease, Oxford. 1977, Blackwell Scit:ntific Publication;,, pp. lRI-218. 16. Roberts, l\L F., Neff. R. K., Hubbell, J. I' .. Taeusch, H. W., and Averv, M. E.: Association herwt"en maternal diabete~ and the respiratory distress smdromc in the newborn,!'\. Engl. J. Med. 294:35i, 1976. I 7. Liggins. G. C .. and Howie, R. !\. A.: Controlled trial ol antepartum glucocorticoid treatment for prevention of the respiratorY distress syndrome in the premature infants. Pediatrics 50:515. 1972.