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Comparison of continuous transcutaneous and continuous intravascular Po 2 measurement in fetal sheep
Comparison of continuous transcutaneous and continuous intravascular Po2 measurement in fetal sheep .._ C. A. M. JANSEN Leiden, Holland
FIONA G. BASS K. C. LOWE P. W. NATHANIELSZ Torrance, California Continuously monitored carotid arterial Po 2 (P8o,) and transcutaneous Po 2 (tcPo 2) from the scalp of fetuses from ewes not in labor have been compared under epidural anesthesia at different levels of fetal oxygenation. A reasonably good correlation existed between the two readings at normal and high Po2 values. In sharp contrast, at low Pao, levels there was a considerable bias between the two. Since this bias was variable, the failure of tcPo2 to reflect Pao, accurately at low Pao, renders the use of the tcPo2 electrode questionabie in the very situation for which it was advocated, nameiy, the prediction of fetal compromise. (AM. J. OBSTET. GYNECOL. 138:670, 1980.)
feral asphyxia is probably the major cause of preventable perinatal mortality and morbidity. The prediction and accurate assessment of intrapartum fetal asphyxia would be of considerable practical use in obstetrics. Transcutaneous Po2 (tcPo 2 ) measurement by means of a thermostatically heated electrode placed upon the fetal scalp has been practiced as a method of intrapartum fetal monitoring.' In this study of 51 patients, a correlation was observed between various parameters of fetal heart rate and tcPo 2 • We previously reported the use of a continuously recording intravascular Po 2 electrode for up to 41 days in the chronicaily catheterized fetal sheep preparaiion and demonstrated continuous variability in fetal Po 2 • 2 The accuracy with which continuous tcPo 2 readings reflect continuous variability in fetal vascular Po2 has not been determined. Therefore, we compared the values obtained under epidural anesthesia from the INTRAPARTUM
From the Department of Obstetrics and Gynecology, University Hospital, Leiden, and the Department of Obstetrics and Gynecology, University of California at Los Angeles School of Medicine, Harbor General Hospital, Torrance. Sponsored by the Society for Gynecologic Investigation. Reprint requests: C. A. M. jansen, Department of Obstetrics and Gynecology, University Hospital, Leiden, Rijnsburgerweg 10, Leiden, The Netherlands.
670
continuously recording Po 2 electrode located in the fetal carotid artery (Pa 0 ,) and those from a transcutaneous electrode applied to the scalp of the feral sheep. No previous comparison has been reported in the literature for continuously recorded tcPo2 and Pao, in the fetus. In addition, the present study was performed without the complication of general anesthesia. The present investigation was conducted in order to provide data that will assist in the correct evaluation of tcPo2 in relation to Pao, under different conditions. The findings also throw light on the physiologic changes that occur in cutaneous blood flow in the fetus under differing levels of fetal oxygenation.
Methods Eight date-mated pregnant Rambouillet-Columbia ewes at 108 to 133 days' gestation were used for this study. Catheters were placed at various points in the fetal circulation and in the amniotic cavity. 2• 3 i\ continuously recording intravascular Po2 electrode was placed in the fetal carotid artery. 2 At least 5 days after the first surgical procedure, a second one was performed. The ewes were sedated with an intramuscular dose of 10 mg of 2.6 xylidine dihydrothiazine (Rompun, Bayer). Thirty minutes later, epidural anesthesia was achieved with the administration of 5.0 ml of 2% (w/v) lignocaine (Xylocaine, Astra) and 5.0 ml of 0.5% 0002-9378/80/220670+07$00.70/0
©
1980 The C. V. Mosby Co.
Volume ns Number !i
Continuous Po, measurement
671
Table I. Fetal and maternal pH and blood gas values* At swrt of premedication
At start of experiment
After hyperoxia
After hypoxia
.It end of experiment
Fetal pH Fetal Pcoz Fetal Po2
7.35 ± 0.05 44.8 ± 5.4 19.1 ± 3.6
7.21 ± 0.09 50.8 ± 6.4 17.6±3.6
7.17±0.10 51.4±11.1 16.:l ± 4.1
7.16 ± O.OR S4.5 ± 10.2 15.4 ± 4.0
701 ± O.H 6'>.2 ± 19.4 I \.6 ± 4.3
Maternal pH Maternal Pco 2 Maternal Po 2
7.47±0.03 31.6 ± 3.0 98.5 ± 6.5
7.49 ± 0.02 33.6 ± 2.9 75.8 ± 16.9
7.48 ± 0.02 30.4 ± 5.0 65.0 ± 14.4
i.4R ± 0.03 :H. I± 2.5 i 1.0 ± 8.4
7 18 ± O.O:l :l7.\l ± 7.4 6!.2 ± 16.1
*Mean ± SD; n = 3 to 7 as described under "Results," during the experimental protocol. Samples of fetal blood were drawn from the carotid artery, and samples of maternal blood were obtained from the femoral artery at the start of premedication, after stabilization of the Po 2 electrode, after the hyperoxia procedure, after the hypoxia procedure, and at the end of the <·xpcrimcnt.
(w/v) bupivacaine (Marcaine, B.D.H.). With the ewe placed in a supine position, the uterus was exposed via a lower midline abdominal incision. After the maternal abdomen had been opened, the fetal head was located, and in order to make a uterine window of about 5 em in diameter, an incision was made through the uterus at a position that was free of cotyledons. The occipital area of the fetal head was approximated against the incision to prevent the loss of amniotic fluid. A relatively Hat area of the scalp was shaved and a transcutaneous Po2 electrode, developed by Huch and associates' and commercially available from Drager, West Germany, was fixed to the fetal skin with a cyanoacrylate glue. The technical details of this electrode have been extensively reported elsewhere.' The Drager tcPo 2 electrode was chosen because it is reportedly superior to commercially available alternatives.4 The electrode was heated to 44° C, and the. relative heating energy required to produce this stabilization was recorded continuously. At least 30 minutes were allowed to elapse after placement in order to permit stabilization of the tcPo 2 • After stabilization of the tcPo 2 electrode output, the responses to three experimental protocols were examined in a fixed order: first, with the ewe breathing I 00% 0 2 (I 2 Llmin) through a transparent plastic bag over her head (hyperoxia studies); second, with the ewe breathing 9% 0 2 and 3% C0 2 in N 2 (12 Llmin) (hypoxia studies); and, finally, with clamping of the umbilical cord for 1 minute during the administration of 100% 0 2 ( 12 L/min) to the ewe. The period of exposure to maternal hyperoxia was 20 minutes, followed by a period of 20 minutes in which the ewe breathed room air. Ewes were exposed to hyperoxia from two to four times. The protocol for the hypoxia experiments was similar to that for hyperoxia, with the exception that the exposure of the mother to the low Po 2 gas mixture lasted only 15 minutes. Pa 0 , values read from the traces as described in Figs. 1 and 2 were pooled in
each animal at equivalent times relating to the exposure. The percentage of oxygen in the plastic bag was monitored by means of a Teledyne oxygen controller (Teledyne Analytical Instruments). At the termination of the hypoxia experiments, the ewes were allowed to breathe room air for ~0 minutes. After this 20-minute period, 100% oxygen was administered to the ewe, and the umbilical cord was located through the uterine incision. After a stable period of at least 10 minutes, the umbilical cord was occluded for 60 seconds. After at least 10 minutes, the occlusion was repeated at least twice on each fetus. The total duration of the experiments was between 3 and 5 hours. The response time of both electrodes wa~ measured in vitro both before and after the experiment. All of the Pa 0 , electrodes used had 95% deflection times of I 0 to 15 seconds and the transcutaneous (tc) electrodes had a 95% deflection time of 15 to 22 seconds. Samples of fetal blood were taken at frequent inten als to ensure correct reading of the Po 2 electrode. Data are presented throughout as mean ± SD. Results
All eight intravascular Po2 electrodes were functioning at the start of the second surgical procedure. One intravascular electrode ceased recording for unexplained reasons before, and one during, the maternal hyperoxia experiments. Five of the eight transcutaneous electrodes fulfilled the criteria of Huch and associates1 after application to the fetal scalp, namely, there was an immediate fall from atmospheric Po 2 within 3 to 5 minutes followed by an increase to a plateau within 20 minutes during thermal heating. In one of these five preparations, the intravascular Po 2 electrode stopped working, as described above. Therefore, a direct comparison between both continuous traces was possible in only four fetuses. Three of the eight transcutaneous electrodes failed to function adequately. One reading was zero Po 2 throughout the whole experirnent. 1\n-
672 Jansen et aL
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Fig. 1, C. Ratio of mean tcPo 2 obtained at different Pa 0 , values in four fetal sheep at 114 to 139 days' gestation. The total number of data points for the four animals was 79 (6), 35 (o), 25 (V'), and 102 (o) Pa0 , represents the mean of values taken during a 2-minute epoch; the highest tcPo2 during that period was recorded at a given Pa0 ,. Mean tcPo2 was calculated from the tcPo 2 values measured. Fetus \7; pH range was 7.34 to 7.26; Fetus o: pH range was 7.13 to 7.10; Fetus o: pH range was 7.30 to 7.10; Fetus 6: pH range was 7.13 to 7.12.
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Condition of the fetuses during the experimental protocols. The fetal and maternal pH, Pco 2 , and Pa 0 ,
B Pa02 mmHg
Fig. l,A and B. A, Comparison of simultaneous measurement of maximum transcutaneous (tc) Po2 in 2-minute epochs and
mean Pa0 , over the same period measured with an indwelling intravascular electrode in four fetal sheep at 114 to 139 days' gestation. Individual symbols represent individual animals, and the numbers represent points at which there was more
than one observation. Values obtained during the rapidly
changing phase in the first 6 minutes after alteration of the gas mixture inhaled by the ewe and at all times during the cord clamping experiment were not included in Fig. l. Mean ± SD of Pa0 , values at given tcPo2 values. Data and details as for A. other reading was zero Po 2 except during the hyperoxia experiment, when the reading reached a maximum of 6 mm Hg. A third transcutaneous electrode was rejected since it reached its nadir after 5 minutes of
throughout the experiment are shown in Table I. Premedication, epidural anesthesia, and the placement of the ewe in the supine position followed by the surgical procedures described resulted in a fall in fetal pH, although this fall was not statistically significant (p > 0.05), and a fall in maternal Po 2 , with no marked change in any of the other variables. During the hyperoxia and hypoxia perturbations, there were no marked changes other than a further fall in mean fetal pH of 0.05 mm Hg.
Direct comparison of tcPoz and Pao2 in hyperoxic, normoxic, and hypoxic conditions. Fig. l, A, demonstrates the individual gas tensions taken at 2-minute intervals read from the continuous trace as described above. These data were obtained from four fetuses in which a direct comparison between the Pa 0 , and tc electrodes was possible. All data points were obtained while the fetus was in a stable condition at least 6 minutes after any change in the composition of the mixtures
Continuous Po 2 measurement
Volume 138 !\umber 6
673
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i" E E
6
TIME (Minutes)
Fig. 2A. Mean:±: SD of Pao, (o----o) (n = 7) and tcPo 2 ( • - - • ) (n = 5) before and during the initial
phase of maternal inspiration of 100% oxygen. After a 20-minute period of breathing this gas mixture. the recovery phase is shown. "'E
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Fig. 2B. Mean:!: SD of Pao, (o----o) (n = 3) and tcPo 2 ( • - - • ) (n = 2) before and during the initial phase of maternal inspiration of 9% oxygen with 3% C0 2 • After a 15-minute period of breathing this gas mixture. the recovery phase is shown. Point zero was taken as the moment when the new equilibrium in the bag was reached. inhaled by the ewe. P~ values obtained during equilibrium in response to different gas mixtures are discussed separately below. No data from the cord clamping experiments are included. Fig. l, A and B, demonstrates dearly that the divergence of tcPo2 from Pa0 , increases as Pao, falls. This observation is also well demonstrated when the ratio of tcPo 2 is plotted against Pa0 , (Fig. 1, C). In all four fetuses this ratio was always less than I, even during maternal hyperoxia, and fell as
fetal Pao, decreased. In one fetus the ratio was always less than 0.5, which was considerably less than that in the other three fetuses. The low value in this animal did not seem to be due solely to the low pH, since another fetus also had the same pH. As the experiments progressed, there was a tendency for the overall ratio of tcPo 2 to Pao, to fall. In a comparable situation, the mean ratio in the first hyperoxia experiment and the hyperoxia immediately prior to the cord clamping
674 Jansen et al.
November 15. 19~0 Am.]. Obstet. Gvnecol.
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Fig. 3A. Response of fetal Pao, monitored continuously to I minute of cord clamping in four fetal sheep at 114 to 139 days' gestation. Each point represents the mean ± SD of three to five episodes.
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tcPoz was above 9 mm Hg, and in one fetus in which the Pa 0 , electrode alone was working (Fig. 2B). The increases in Pa 0 , and tcPo 2 during maternal h)peroxia were similar. The maximum increases in Pa 0 , and tcPo 2 were 1.64 ± 0.65 mm Hg min- 1 (n = i) and l. 78 ± 0. 70 mm Hg min- 1 (n = 5), respectively. The maximum declines from the plateaus when the ewe inhaled room air were 2.23 ± 0.45 mm Hg min 1 (n = 7) for the Pa 0 , electrode and 2.1 ± 0.65 mm Hg min-t (n = 5) for the tcPo 2 electrode. The maximum changes during maternal hypoxia were a fall of 2 ± 0.87 mm Hg min- 1 (n = 3) for Pa 0 , and 3.0 (mean of 2) mm Hg min- 1 for the tcPo 2 electrode. When the ewe breathed room air, the Pa 0 , electrode reading rose maximally, 2.1 ± 0.2 mm Hg min- 1 (n = 3), and the tcPo 2 rose 3.0 mm Hg min- 1 (mean of 2).
Response of tcP02 to clamping the umbilical cord for 1 minute. Figs. 3A and 3B illustrate the response of four fetuses to clamping the umbilical cord for 1 minute. The response of Pa0 , was statistically significant at 10 seconds (p < 0.05). The fall in tcPo 2 occurred more slowly, and in none of the fetuses did the tcPo 2 fall significantly within the first 10 seconds. The differences in the recovery period were even more marked. Pa 0 , returned to normal within lO seconds, whereas recovery of tcPo 2 to its initial levels required up to 5 minutes. Relative heating power. The relative energy required to keep the temperature of the electrodes stable at a plateau of 44° C, which is said to be an indicator of the state of vasodilation in the skin below the electrode, did not reveal any recognizable pattern during any part of the experimental protocol.
Comment
Fig. 38. Response of fetal tcPo 2 to I minute of cord clamping (as in Fig. 3A).
in the four animals was: 0.92 and 0.84 (V), 0.42 and 0.20 (b.), 0.86 and 0.78 (o), and 0.88 and 0.32 (o). Response to maternal inhalation of different gas mixtures. The response during maternal hyperoxia was observed in all seven preparations in which the Pa 0 , electrodes were working and in all five in which the tcPo 2 electrodes were functioning (Fig. 2A). The exposure of the ewe to hypoxia was performed in the two preparations with functional tcPo2 electrodes in w·hich
Since the tcPo 2 electrode has been advocated for the at-risk fetus, despite the lack of experimental data, in order to assess its clinical usefulness, we investigated the effects of hyperoxia and hypoxia on the correlation between the Pa 0 , and tcPo 2 • The fetal pH and Pa 0 , values that existed after the procedures which were required for the placement of the transcutaneous electrode were similar to those observed in many at-risk human fetuses. To our knowledge, no previous comparison has been made of these two continuously recording methods of monitoring fetal oxygenation. In one study in which a comparison was made between tcPo 2 and samples of blood obiained interrnittently fron1 the fetal carotid artery, a good correlation was observed over the range of 1 A
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Volume 13R Number 6
samples nor the period of exposure to different gas mixtures (approximately 5 minutes) was specified. In one figure, tcPo 2 was shown to fall to nearly zero; however, no values lower than 14 mm Hg were used in the correlation between Pa 0 , and tcPo 2 • In another study, in two fetuses under general anesthesia with Ethrane, the same comparison of intermittent Pa 0 , and continuous tcPo 2 yielded an r = 0.977 and a slope of 0.89. 6 Only two of the 18 points used for this calculation were at a Pa 0 , of less than 14 mm Hg. The remainder ranged from 14 to 34 mm Hg. Ethrane is a halogenated hydrocarbon, and anesthetics of this group, including halothane, have been shown to be polarographically reduced at Po 2 electrodes 7- 9 and are best avoided when one is making measurements of Po 2 • In addition, general anesthesia of the fetus may affect the level of peripheral vasoconstriction, thereby modifying any disparity between tcPo 2 and Pa 0 , measurements wherever this might otherwise exist. All forms of anesthesia, general and regional, may modify fetal oxygenation and regional blood flow. In one study of newborn monkeys sedated with Sernylan (phencyclidine HCI), tcPo 2 and Pa 0 , correlated well at a Pa 0 , of 70 mm Hg and above, but when Pa 0 , was lowered to 25 mm Hg, tcPo 2 fell to zero. 10 These results in the newborn animal show a similarity to the disparity that we have demonstrated at low Po 2 in the fetus. The changes in fetal Pa 0 , that we have observed during and after maternal hyperoxia agree partly with observations published previously by Matalon and associates.11 They observed a slightly different rate of increase in Pa 0 ,, 2.44 mm Hg min- 1versus our finding of 1.64 mm Hg min,- 1 and decrease, 1.63 mm min- 1 versus our finding of 2.23 mm min.-' However, the conditions of their experiment differed considerably; in particular, the ewes were under general anesthesia with tracheal intubation and were mechanically ventilated. l t is of interest that Pa 0 , readings from the intravascular electrode at 1 minute after occlusion of the umbilical cord were lower than those previously reported in the literature.' 2 The Pa 02 values obtained from the indwelling intravascular Pa 0 , electrode were almost certainly superior to those obtained from samples of blood measured extracorporeally, for two reasons. First, in our experience, accurate assessment of very low Po 2 values necessitates specific calibration in the low range. This observation is in accordance with other reports in the literature, in which a blood gas analyzer in 100% N 2 gas flow read 11 ::': 1.4 mm Hg Po 2 . 13 Second, for practical reasons, during intermittent sampling under experimental conditions in an
Continuous Po 2 measurement
675
animal research laboratory, it is extremeh rlifhcnlt to obtain blood under the absolutely anaerobic conditions necessary to measure low blood Po" accuratdr. The zero Po2 leakage current was always determined in 0111 electrodes both before the insertion and after the experiment, and the reading was corrected for 1his \alue. Our data subsequent to occlusion of the umbilical cord bear resemblance to published data on the delayed response of the transcutaneous Po 2 after restoration of fetal blood flow. 1"'ln this study, fetal oxygenation was impeded by occlusion of the maternal aorta, and after a 2-minute period of occlusion the transcutaneous Po 2 required about 10 minutes to reach its original value. However, the recorded htll in tcPoz was to 6 mm Hg, whereas the intra-arterial Po 2 • calculated from the oxygen saturation, fell to nearlv Lero. The tcPo2 value of 6 mm Hg can be explained solelv by the halothane effect, whereas the oXYgen saturation will not be influenced by halothane. The divergence of Pa,h at low Po 2 during hypoxia and the cord clamping experiments was most likely due to vasoconstriction in the skin. Pronounced peripheral vasoconstriction in the carcass in response to hypoxemia, accompanied by similar levels of acidemia (pH 7.28), has been observed. 15 Peripheral vasoconstriction in response to hypoxemia would enable hlood to be redistributed to more vital organs. We were unable to associate relative hearing power with any changes in Pa 0 ,. Changes in the relative healing power have been suggested as an indicator of fetal peripheral vasoconstriction, but it vielded no useful information in our study. We have observed both in the experimental and in the clinical obstetric sit nation that the relative heating power changed when the electrode was touched during vaginal examination. The dose correlation demonstrated between the relative heating power and uterine contractions during labor in the human being may well be artifactual and not reflect physiologic changes in relative local perfusion. Our experiments were designed to eliminate extraneous physical factors, such as the so-called tonsure effect of the cervix, 16 the presence of a caput succedaneum, and pressure upon the electmde. It is difficult to assess the contribution that these factors might make to tcPo 2 measurements in the human fetu> during labor, but pressures as low as :10 to ll :1 grams (equivalent to 8 to 13 mm Hg) upon the electrode placed upon the scalp of two adults reduced the reading to zero. ' 7 However, since the avascular layer in the adult skin is much thicker. tcPo2 readings in this situation are much lower than the intra-arterial Po 2 . In this study, intra-arterial Po 2 was not measured. If '>W: as-
676 Jansen et al. Am.
sume a value of 100 mm Hg for Pa 0 , the initial ratio of tcPo 2 to Pa 0 , was only 0.14 and 0.38, so that extrapolation from adults to neonates or fetuses is probably inappropriate. In conclusion, we have demonstrated a pronounced
REFERENCES I. Huch, A., Huch, R., Schneider, H., and Rooth, G.: Continuous transcutaneous monitoring of fetal oxygen tension during labour, Br. J. Obstet. Gynaecol. (Suppl I) 84:1, 1977. 2. Jansen, C. A. M., Krane, E. J., Thomas, A. L., Beck, N. F. G., Lowe, K. C., Joyce, P., Parr, M., and Nathanielsz, P. W.: Continuous variability of fetal Poz in the chronically catheterized fetal sheep, AM. J. OssTET. GYNECOL. 134:776, 1979. 3. Nathanielsz, P. W., Abel, M. H., Bass, F. G., Krane, E. J., Thomas, A. L., and Liggins, G. C.: Pituitary stalk section and some of its effects on endocrine function in the fetal lamb, Q. J. Exp. Physiol. 63:211, 1978. 4. Le Souef, P. N., Morgan, A. K., Sautter, L. P., Reynolds, E. 0. R., and Parker, D.: Continuous comparison of transcutaneous and arterial oxygenation in newborn infants with respiratory illnesses, Acta Anaesthesia!. Scand. (Suppi.)68:91, 1978. 5. Mueller-Heubach, E., Seiler, D., Huch, R., and Huch, A.: Use of the tcPoz electrode in the animal fetus, Birth Defects 15(4):599, 1979. 6. Hof, D. van 't, Wladimiroff, J. W., Wallenburg, H. C. S., and Drogendijk, A. C.: Simultaneous measurement of transcutaneous and central arterial Paz in the acute sheep experiment, Birth Defects 15(4):615, 1979. 7. Severinghaus,J. W., Weiskopf, R. B., Nishimura, M., and Bradley, A. F.: Oxygen electrode errors due to polarographic reduction of halothane, J. Appl. Physiol. 31:640, 1971. 8. Dent, J. G., and Netter, K. J.: Errors in oxygen tension measurements caused by halothane, Br. J. Anaesth. 48:195, 1976.
November 15, 1980 J. Obstet. Gynewl.
and unpredictable bias between tcPo 2 and Pa 0 , aL low fetal Pa0 , levels. Clinically, the tcPo 2 electrode has been advocated for use in the at-risk fetus. Our data strongly question the value of this electrode in the hypoxic fetus.
9. Gothgen, 1., and Jacobsen, E.: Transcutaneous oxygen tension measurement. II. The influence of halothane and hypotension, Acta Anaesthesia!. Scand. (Suppl.)67:71, 1978. 10. Johnson, P. L., Wilkinson, A. R., Sloper, J., and Whyte, P. L.: Continuous transcutaneous and intra-arterial oxygen measurement during experimental hypoxemia in infant monkeys, Birth Defects 15(4):607, 1979. II. Matalon, S. V., Manning, P. J., Bernie, B. J., Eichorst, B. C., Hunt, C. E., and Seeds, A. E.: The effect of changes of maternal Pao, on the fetal Pa0 ,-in vivo study, Respir. Physiol. 32:51, 1978. 12. Daniel, S. S., Huzain, M. K., Milliez, T•• Stark, R. 1., Yeh, M. N ., and James, L. S.: Renal resp;nse of fetal lamb to complete occlusion of umbilical cord, AM. J. OBSTF.T. GYNECOL.
131:514, 1978.
13. Bates, M. L., Feingold, A., and Gold, M. 1.: The effects of anesthetics on an in vivo oxygen electrode, Am. J. Clin. Pathoi. 64:448, 1975. 14. Kiinzel, W., Kastendieck, E., and Kurz, C. S.: A comparative study of continuous intravascular Oz saturation and transcutaneous Paz measurement in the sheep fetus following the reduction of uterine blood flow, Birth Defects 15(4):591, 1979. 15. Cohn, H. E., Sacks, E.J., Heymann, M.A., and Rudolph. A. M.: Cardiovascular responses to hypoxemia and acidemia in fetal lambs, AM. J. 0BSTET. GYNECOL. 120:817, 1974. 16. O'Connor, M. C., and Hytten, F. E.: Measurement of transcutaneous oxygen tension-Problems and potential, Br. J. Obstet. Gynaecol. 86:948, 1979. 17. O'Connor, M. C., Hytten, F. E., and Zanelli, G. D.: Is the fetus "scalped" in labour? Lancet 2:947, 1979.
FIONA G. BASS K. C. LOWE P. W. NATHANIELSZ Torrance, California Continuously monitored carotid arterial Po 2 (P8o,) and transcutaneous Po 2 (tcPo 2) from the scalp of fetuses from ewes not in labor have been compared under epidural anesthesia at different levels of fetal oxygenation. A reasonably good correlation existed between the two readings at normal and high Po2 values. In sharp contrast, at low Pao, levels there was a considerable bias between the two. Since this bias was variable, the failure of tcPo2 to reflect Pao, accurately at low Pao, renders the use of the tcPo2 electrode questionabie in the very situation for which it was advocated, nameiy, the prediction of fetal compromise. (AM. J. OBSTET. GYNECOL. 138:670, 1980.)
feral asphyxia is probably the major cause of preventable perinatal mortality and morbidity. The prediction and accurate assessment of intrapartum fetal asphyxia would be of considerable practical use in obstetrics. Transcutaneous Po2 (tcPo 2 ) measurement by means of a thermostatically heated electrode placed upon the fetal scalp has been practiced as a method of intrapartum fetal monitoring.' In this study of 51 patients, a correlation was observed between various parameters of fetal heart rate and tcPo 2 • We previously reported the use of a continuously recording intravascular Po 2 electrode for up to 41 days in the chronicaily catheterized fetal sheep preparaiion and demonstrated continuous variability in fetal Po 2 • 2 The accuracy with which continuous tcPo 2 readings reflect continuous variability in fetal vascular Po2 has not been determined. Therefore, we compared the values obtained under epidural anesthesia from the INTRAPARTUM
From the Department of Obstetrics and Gynecology, University Hospital, Leiden, and the Department of Obstetrics and Gynecology, University of California at Los Angeles School of Medicine, Harbor General Hospital, Torrance. Sponsored by the Society for Gynecologic Investigation. Reprint requests: C. A. M. jansen, Department of Obstetrics and Gynecology, University Hospital, Leiden, Rijnsburgerweg 10, Leiden, The Netherlands.
670
continuously recording Po 2 electrode located in the fetal carotid artery (Pa 0 ,) and those from a transcutaneous electrode applied to the scalp of the feral sheep. No previous comparison has been reported in the literature for continuously recorded tcPo2 and Pao, in the fetus. In addition, the present study was performed without the complication of general anesthesia. The present investigation was conducted in order to provide data that will assist in the correct evaluation of tcPo2 in relation to Pao, under different conditions. The findings also throw light on the physiologic changes that occur in cutaneous blood flow in the fetus under differing levels of fetal oxygenation.
Methods Eight date-mated pregnant Rambouillet-Columbia ewes at 108 to 133 days' gestation were used for this study. Catheters were placed at various points in the fetal circulation and in the amniotic cavity. 2• 3 i\ continuously recording intravascular Po2 electrode was placed in the fetal carotid artery. 2 At least 5 days after the first surgical procedure, a second one was performed. The ewes were sedated with an intramuscular dose of 10 mg of 2.6 xylidine dihydrothiazine (Rompun, Bayer). Thirty minutes later, epidural anesthesia was achieved with the administration of 5.0 ml of 2% (w/v) lignocaine (Xylocaine, Astra) and 5.0 ml of 0.5% 0002-9378/80/220670+07$00.70/0
©
1980 The C. V. Mosby Co.
Volume ns Number !i
Continuous Po, measurement
671
Table I. Fetal and maternal pH and blood gas values* At swrt of premedication
At start of experiment
After hyperoxia
After hypoxia
.It end of experiment
Fetal pH Fetal Pcoz Fetal Po2
7.35 ± 0.05 44.8 ± 5.4 19.1 ± 3.6
7.21 ± 0.09 50.8 ± 6.4 17.6±3.6
7.17±0.10 51.4±11.1 16.:l ± 4.1
7.16 ± O.OR S4.5 ± 10.2 15.4 ± 4.0
701 ± O.H 6'>.2 ± 19.4 I \.6 ± 4.3
Maternal pH Maternal Pco 2 Maternal Po 2
7.47±0.03 31.6 ± 3.0 98.5 ± 6.5
7.49 ± 0.02 33.6 ± 2.9 75.8 ± 16.9
7.48 ± 0.02 30.4 ± 5.0 65.0 ± 14.4
i.4R ± 0.03 :H. I± 2.5 i 1.0 ± 8.4
7 18 ± O.O:l :l7.\l ± 7.4 6!.2 ± 16.1
*Mean ± SD; n = 3 to 7 as described under "Results," during the experimental protocol. Samples of fetal blood were drawn from the carotid artery, and samples of maternal blood were obtained from the femoral artery at the start of premedication, after stabilization of the Po 2 electrode, after the hyperoxia procedure, after the hypoxia procedure, and at the end of the <·xpcrimcnt.
(w/v) bupivacaine (Marcaine, B.D.H.). With the ewe placed in a supine position, the uterus was exposed via a lower midline abdominal incision. After the maternal abdomen had been opened, the fetal head was located, and in order to make a uterine window of about 5 em in diameter, an incision was made through the uterus at a position that was free of cotyledons. The occipital area of the fetal head was approximated against the incision to prevent the loss of amniotic fluid. A relatively Hat area of the scalp was shaved and a transcutaneous Po2 electrode, developed by Huch and associates' and commercially available from Drager, West Germany, was fixed to the fetal skin with a cyanoacrylate glue. The technical details of this electrode have been extensively reported elsewhere.' The Drager tcPo 2 electrode was chosen because it is reportedly superior to commercially available alternatives.4 The electrode was heated to 44° C, and the. relative heating energy required to produce this stabilization was recorded continuously. At least 30 minutes were allowed to elapse after placement in order to permit stabilization of the tcPo 2 • After stabilization of the tcPo 2 electrode output, the responses to three experimental protocols were examined in a fixed order: first, with the ewe breathing I 00% 0 2 (I 2 Llmin) through a transparent plastic bag over her head (hyperoxia studies); second, with the ewe breathing 9% 0 2 and 3% C0 2 in N 2 (12 Llmin) (hypoxia studies); and, finally, with clamping of the umbilical cord for 1 minute during the administration of 100% 0 2 ( 12 L/min) to the ewe. The period of exposure to maternal hyperoxia was 20 minutes, followed by a period of 20 minutes in which the ewe breathed room air. Ewes were exposed to hyperoxia from two to four times. The protocol for the hypoxia experiments was similar to that for hyperoxia, with the exception that the exposure of the mother to the low Po 2 gas mixture lasted only 15 minutes. Pa 0 , values read from the traces as described in Figs. 1 and 2 were pooled in
each animal at equivalent times relating to the exposure. The percentage of oxygen in the plastic bag was monitored by means of a Teledyne oxygen controller (Teledyne Analytical Instruments). At the termination of the hypoxia experiments, the ewes were allowed to breathe room air for ~0 minutes. After this 20-minute period, 100% oxygen was administered to the ewe, and the umbilical cord was located through the uterine incision. After a stable period of at least 10 minutes, the umbilical cord was occluded for 60 seconds. After at least 10 minutes, the occlusion was repeated at least twice on each fetus. The total duration of the experiments was between 3 and 5 hours. The response time of both electrodes wa~ measured in vitro both before and after the experiment. All of the Pa 0 , electrodes used had 95% deflection times of I 0 to 15 seconds and the transcutaneous (tc) electrodes had a 95% deflection time of 15 to 22 seconds. Samples of fetal blood were taken at frequent inten als to ensure correct reading of the Po 2 electrode. Data are presented throughout as mean ± SD. Results
All eight intravascular Po2 electrodes were functioning at the start of the second surgical procedure. One intravascular electrode ceased recording for unexplained reasons before, and one during, the maternal hyperoxia experiments. Five of the eight transcutaneous electrodes fulfilled the criteria of Huch and associates1 after application to the fetal scalp, namely, there was an immediate fall from atmospheric Po 2 within 3 to 5 minutes followed by an increase to a plateau within 20 minutes during thermal heating. In one of these five preparations, the intravascular Po 2 electrode stopped working, as described above. Therefore, a direct comparison between both continuous traces was possible in only four fetuses. Three of the eight transcutaneous electrodes failed to function adequately. One reading was zero Po 2 throughout the whole experirnent. 1\n-
672 Jansen et aL
Am.
1\ovember 15. lLJHO J. Obstet. Gvneml.
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Fig. 1, C. Ratio of mean tcPo 2 obtained at different Pa 0 , values in four fetal sheep at 114 to 139 days' gestation. The total number of data points for the four animals was 79 (6), 35 (o), 25 (V'), and 102 (o) Pa0 , represents the mean of values taken during a 2-minute epoch; the highest tcPo2 during that period was recorded at a given Pa0 ,. Mean tcPo2 was calculated from the tcPo 2 values measured. Fetus \7; pH range was 7.34 to 7.26; Fetus o: pH range was 7.13 to 7.10; Fetus o: pH range was 7.30 to 7.10; Fetus 6: pH range was 7.13 to 7.12.
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Condition of the fetuses during the experimental protocols. The fetal and maternal pH, Pco 2 , and Pa 0 ,
B Pa02 mmHg
Fig. l,A and B. A, Comparison of simultaneous measurement of maximum transcutaneous (tc) Po2 in 2-minute epochs and
mean Pa0 , over the same period measured with an indwelling intravascular electrode in four fetal sheep at 114 to 139 days' gestation. Individual symbols represent individual animals, and the numbers represent points at which there was more
than one observation. Values obtained during the rapidly
changing phase in the first 6 minutes after alteration of the gas mixture inhaled by the ewe and at all times during the cord clamping experiment were not included in Fig. l. Mean ± SD of Pa0 , values at given tcPo2 values. Data and details as for A. other reading was zero Po 2 except during the hyperoxia experiment, when the reading reached a maximum of 6 mm Hg. A third transcutaneous electrode was rejected since it reached its nadir after 5 minutes of
throughout the experiment are shown in Table I. Premedication, epidural anesthesia, and the placement of the ewe in the supine position followed by the surgical procedures described resulted in a fall in fetal pH, although this fall was not statistically significant (p > 0.05), and a fall in maternal Po 2 , with no marked change in any of the other variables. During the hyperoxia and hypoxia perturbations, there were no marked changes other than a further fall in mean fetal pH of 0.05 mm Hg.
Direct comparison of tcPoz and Pao2 in hyperoxic, normoxic, and hypoxic conditions. Fig. l, A, demonstrates the individual gas tensions taken at 2-minute intervals read from the continuous trace as described above. These data were obtained from four fetuses in which a direct comparison between the Pa 0 , and tc electrodes was possible. All data points were obtained while the fetus was in a stable condition at least 6 minutes after any change in the composition of the mixtures
Continuous Po 2 measurement
Volume 138 !\umber 6
673
24
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6
TIME (Minutes)
Fig. 2A. Mean:±: SD of Pao, (o----o) (n = 7) and tcPo 2 ( • - - • ) (n = 5) before and during the initial
phase of maternal inspiration of 100% oxygen. After a 20-minute period of breathing this gas mixture. the recovery phase is shown. "'E
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Fig. 2B. Mean:!: SD of Pao, (o----o) (n = 3) and tcPo 2 ( • - - • ) (n = 2) before and during the initial phase of maternal inspiration of 9% oxygen with 3% C0 2 • After a 15-minute period of breathing this gas mixture. the recovery phase is shown. Point zero was taken as the moment when the new equilibrium in the bag was reached. inhaled by the ewe. P~ values obtained during equilibrium in response to different gas mixtures are discussed separately below. No data from the cord clamping experiments are included. Fig. l, A and B, demonstrates dearly that the divergence of tcPo2 from Pa0 , increases as Pao, falls. This observation is also well demonstrated when the ratio of tcPo 2 is plotted against Pa0 , (Fig. 1, C). In all four fetuses this ratio was always less than I, even during maternal hyperoxia, and fell as
fetal Pao, decreased. In one fetus the ratio was always less than 0.5, which was considerably less than that in the other three fetuses. The low value in this animal did not seem to be due solely to the low pH, since another fetus also had the same pH. As the experiments progressed, there was a tendency for the overall ratio of tcPo 2 to Pao, to fall. In a comparable situation, the mean ratio in the first hyperoxia experiment and the hyperoxia immediately prior to the cord clamping
674 Jansen et al.
November 15. 19~0 Am.]. Obstet. Gvnecol.
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tcPoz was above 9 mm Hg, and in one fetus in which the Pa 0 , electrode alone was working (Fig. 2B). The increases in Pa 0 , and tcPo 2 during maternal h)peroxia were similar. The maximum increases in Pa 0 , and tcPo 2 were 1.64 ± 0.65 mm Hg min- 1 (n = i) and l. 78 ± 0. 70 mm Hg min- 1 (n = 5), respectively. The maximum declines from the plateaus when the ewe inhaled room air were 2.23 ± 0.45 mm Hg min 1 (n = 7) for the Pa 0 , electrode and 2.1 ± 0.65 mm Hg min-t (n = 5) for the tcPo 2 electrode. The maximum changes during maternal hypoxia were a fall of 2 ± 0.87 mm Hg min- 1 (n = 3) for Pa 0 , and 3.0 (mean of 2) mm Hg min- 1 for the tcPo 2 electrode. When the ewe breathed room air, the Pa 0 , electrode reading rose maximally, 2.1 ± 0.2 mm Hg min- 1 (n = 3), and the tcPo 2 rose 3.0 mm Hg min- 1 (mean of 2).
Response of tcP02 to clamping the umbilical cord for 1 minute. Figs. 3A and 3B illustrate the response of four fetuses to clamping the umbilical cord for 1 minute. The response of Pa0 , was statistically significant at 10 seconds (p < 0.05). The fall in tcPo 2 occurred more slowly, and in none of the fetuses did the tcPo 2 fall significantly within the first 10 seconds. The differences in the recovery period were even more marked. Pa 0 , returned to normal within lO seconds, whereas recovery of tcPo 2 to its initial levels required up to 5 minutes. Relative heating power. The relative energy required to keep the temperature of the electrodes stable at a plateau of 44° C, which is said to be an indicator of the state of vasodilation in the skin below the electrode, did not reveal any recognizable pattern during any part of the experimental protocol.
Comment
Fig. 38. Response of fetal tcPo 2 to I minute of cord clamping (as in Fig. 3A).
in the four animals was: 0.92 and 0.84 (V), 0.42 and 0.20 (b.), 0.86 and 0.78 (o), and 0.88 and 0.32 (o). Response to maternal inhalation of different gas mixtures. The response during maternal hyperoxia was observed in all seven preparations in which the Pa 0 , electrodes were working and in all five in which the tcPo 2 electrodes were functioning (Fig. 2A). The exposure of the ewe to hypoxia was performed in the two preparations with functional tcPo2 electrodes in w·hich
Since the tcPo 2 electrode has been advocated for the at-risk fetus, despite the lack of experimental data, in order to assess its clinical usefulness, we investigated the effects of hyperoxia and hypoxia on the correlation between the Pa 0 , and tcPo 2 • The fetal pH and Pa 0 , values that existed after the procedures which were required for the placement of the transcutaneous electrode were similar to those observed in many at-risk human fetuses. To our knowledge, no previous comparison has been made of these two continuously recording methods of monitoring fetal oxygenation. In one study in which a comparison was made between tcPo 2 and samples of blood obiained interrnittently fron1 the fetal carotid artery, a good correlation was observed over the range of 1 A
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Volume 13R Number 6
samples nor the period of exposure to different gas mixtures (approximately 5 minutes) was specified. In one figure, tcPo 2 was shown to fall to nearly zero; however, no values lower than 14 mm Hg were used in the correlation between Pa 0 , and tcPo 2 • In another study, in two fetuses under general anesthesia with Ethrane, the same comparison of intermittent Pa 0 , and continuous tcPo 2 yielded an r = 0.977 and a slope of 0.89. 6 Only two of the 18 points used for this calculation were at a Pa 0 , of less than 14 mm Hg. The remainder ranged from 14 to 34 mm Hg. Ethrane is a halogenated hydrocarbon, and anesthetics of this group, including halothane, have been shown to be polarographically reduced at Po 2 electrodes 7- 9 and are best avoided when one is making measurements of Po 2 • In addition, general anesthesia of the fetus may affect the level of peripheral vasoconstriction, thereby modifying any disparity between tcPo 2 and Pa 0 , measurements wherever this might otherwise exist. All forms of anesthesia, general and regional, may modify fetal oxygenation and regional blood flow. In one study of newborn monkeys sedated with Sernylan (phencyclidine HCI), tcPo 2 and Pa 0 , correlated well at a Pa 0 , of 70 mm Hg and above, but when Pa 0 , was lowered to 25 mm Hg, tcPo 2 fell to zero. 10 These results in the newborn animal show a similarity to the disparity that we have demonstrated at low Po 2 in the fetus. The changes in fetal Pa 0 , that we have observed during and after maternal hyperoxia agree partly with observations published previously by Matalon and associates.11 They observed a slightly different rate of increase in Pa 0 ,, 2.44 mm Hg min- 1versus our finding of 1.64 mm Hg min,- 1 and decrease, 1.63 mm min- 1 versus our finding of 2.23 mm min.-' However, the conditions of their experiment differed considerably; in particular, the ewes were under general anesthesia with tracheal intubation and were mechanically ventilated. l t is of interest that Pa 0 , readings from the intravascular electrode at 1 minute after occlusion of the umbilical cord were lower than those previously reported in the literature.' 2 The Pa 02 values obtained from the indwelling intravascular Pa 0 , electrode were almost certainly superior to those obtained from samples of blood measured extracorporeally, for two reasons. First, in our experience, accurate assessment of very low Po 2 values necessitates specific calibration in the low range. This observation is in accordance with other reports in the literature, in which a blood gas analyzer in 100% N 2 gas flow read 11 ::': 1.4 mm Hg Po 2 . 13 Second, for practical reasons, during intermittent sampling under experimental conditions in an
Continuous Po 2 measurement
675
animal research laboratory, it is extremeh rlifhcnlt to obtain blood under the absolutely anaerobic conditions necessary to measure low blood Po" accuratdr. The zero Po2 leakage current was always determined in 0111 electrodes both before the insertion and after the experiment, and the reading was corrected for 1his \alue. Our data subsequent to occlusion of the umbilical cord bear resemblance to published data on the delayed response of the transcutaneous Po 2 after restoration of fetal blood flow. 1"'ln this study, fetal oxygenation was impeded by occlusion of the maternal aorta, and after a 2-minute period of occlusion the transcutaneous Po 2 required about 10 minutes to reach its original value. However, the recorded htll in tcPoz was to 6 mm Hg, whereas the intra-arterial Po 2 • calculated from the oxygen saturation, fell to nearlv Lero. The tcPo2 value of 6 mm Hg can be explained solelv by the halothane effect, whereas the oXYgen saturation will not be influenced by halothane. The divergence of Pa,h at low Po 2 during hypoxia and the cord clamping experiments was most likely due to vasoconstriction in the skin. Pronounced peripheral vasoconstriction in the carcass in response to hypoxemia, accompanied by similar levels of acidemia (pH 7.28), has been observed. 15 Peripheral vasoconstriction in response to hypoxemia would enable hlood to be redistributed to more vital organs. We were unable to associate relative hearing power with any changes in Pa 0 ,. Changes in the relative healing power have been suggested as an indicator of fetal peripheral vasoconstriction, but it vielded no useful information in our study. We have observed both in the experimental and in the clinical obstetric sit nation that the relative heating power changed when the electrode was touched during vaginal examination. The dose correlation demonstrated between the relative heating power and uterine contractions during labor in the human being may well be artifactual and not reflect physiologic changes in relative local perfusion. Our experiments were designed to eliminate extraneous physical factors, such as the so-called tonsure effect of the cervix, 16 the presence of a caput succedaneum, and pressure upon the electmde. It is difficult to assess the contribution that these factors might make to tcPo 2 measurements in the human fetu> during labor, but pressures as low as :10 to ll :1 grams (equivalent to 8 to 13 mm Hg) upon the electrode placed upon the scalp of two adults reduced the reading to zero. ' 7 However, since the avascular layer in the adult skin is much thicker. tcPo2 readings in this situation are much lower than the intra-arterial Po 2 . In this study, intra-arterial Po 2 was not measured. If '>W: as-
676 Jansen et al. Am.
sume a value of 100 mm Hg for Pa 0 , the initial ratio of tcPo 2 to Pa 0 , was only 0.14 and 0.38, so that extrapolation from adults to neonates or fetuses is probably inappropriate. In conclusion, we have demonstrated a pronounced
REFERENCES I. Huch, A., Huch, R., Schneider, H., and Rooth, G.: Continuous transcutaneous monitoring of fetal oxygen tension during labour, Br. J. Obstet. Gynaecol. (Suppl I) 84:1, 1977. 2. Jansen, C. A. M., Krane, E. J., Thomas, A. L., Beck, N. F. G., Lowe, K. C., Joyce, P., Parr, M., and Nathanielsz, P. W.: Continuous variability of fetal Poz in the chronically catheterized fetal sheep, AM. J. OssTET. GYNECOL. 134:776, 1979. 3. Nathanielsz, P. W., Abel, M. H., Bass, F. G., Krane, E. J., Thomas, A. L., and Liggins, G. C.: Pituitary stalk section and some of its effects on endocrine function in the fetal lamb, Q. J. Exp. Physiol. 63:211, 1978. 4. Le Souef, P. N., Morgan, A. K., Sautter, L. P., Reynolds, E. 0. R., and Parker, D.: Continuous comparison of transcutaneous and arterial oxygenation in newborn infants with respiratory illnesses, Acta Anaesthesia!. Scand. (Suppi.)68:91, 1978. 5. Mueller-Heubach, E., Seiler, D., Huch, R., and Huch, A.: Use of the tcPoz electrode in the animal fetus, Birth Defects 15(4):599, 1979. 6. Hof, D. van 't, Wladimiroff, J. W., Wallenburg, H. C. S., and Drogendijk, A. C.: Simultaneous measurement of transcutaneous and central arterial Paz in the acute sheep experiment, Birth Defects 15(4):615, 1979. 7. Severinghaus,J. W., Weiskopf, R. B., Nishimura, M., and Bradley, A. F.: Oxygen electrode errors due to polarographic reduction of halothane, J. Appl. Physiol. 31:640, 1971. 8. Dent, J. G., and Netter, K. J.: Errors in oxygen tension measurements caused by halothane, Br. J. Anaesth. 48:195, 1976.
November 15, 1980 J. Obstet. Gynewl.
and unpredictable bias between tcPo 2 and Pa 0 , aL low fetal Pa0 , levels. Clinically, the tcPo 2 electrode has been advocated for use in the at-risk fetus. Our data strongly question the value of this electrode in the hypoxic fetus.
9. Gothgen, 1., and Jacobsen, E.: Transcutaneous oxygen tension measurement. II. The influence of halothane and hypotension, Acta Anaesthesia!. Scand. (Suppl.)67:71, 1978. 10. Johnson, P. L., Wilkinson, A. R., Sloper, J., and Whyte, P. L.: Continuous transcutaneous and intra-arterial oxygen measurement during experimental hypoxemia in infant monkeys, Birth Defects 15(4):607, 1979. II. Matalon, S. V., Manning, P. J., Bernie, B. J., Eichorst, B. C., Hunt, C. E., and Seeds, A. E.: The effect of changes of maternal Pao, on the fetal Pa0 ,-in vivo study, Respir. Physiol. 32:51, 1978. 12. Daniel, S. S., Huzain, M. K., Milliez, T•• Stark, R. 1., Yeh, M. N ., and James, L. S.: Renal resp;nse of fetal lamb to complete occlusion of umbilical cord, AM. J. OBSTF.T. GYNECOL.
131:514, 1978.
13. Bates, M. L., Feingold, A., and Gold, M. 1.: The effects of anesthetics on an in vivo oxygen electrode, Am. J. Clin. Pathoi. 64:448, 1975. 14. Kiinzel, W., Kastendieck, E., and Kurz, C. S.: A comparative study of continuous intravascular Oz saturation and transcutaneous Paz measurement in the sheep fetus following the reduction of uterine blood flow, Birth Defects 15(4):591, 1979. 15. Cohn, H. E., Sacks, E.J., Heymann, M.A., and Rudolph. A. M.: Cardiovascular responses to hypoxemia and acidemia in fetal lambs, AM. J. 0BSTET. GYNECOL. 120:817, 1974. 16. O'Connor, M. C., and Hytten, F. E.: Measurement of transcutaneous oxygen tension-Problems and potential, Br. J. Obstet. Gynaecol. 86:948, 1979. 17. O'Connor, M. C., Hytten, F. E., and Zanelli, G. D.: Is the fetus "scalped" in labour? Lancet 2:947, 1979.