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Comparison of fetal scalp, carotid, and jugular blood gas values and oxygen consumption in the lamb
FETUS, PLACENTA, AND NEWBORN
Comparison of fetal scalp, carotid, and jugular blood gas values and oxygen consumption in the lamb R.
W.
P.
V.
SHIER, DILTS,
Lexington,
M.D. JR.,
M.D.
Kentucky
Scalp pH, PO*, Pcog, and base-deficit values in the fetal lamb are cornbared to the same values in fetal carotid arterial and jugular venous blood and to fetal cephalic blood flow, oxygen consumption, blood pressure, and heart rate during control, hypoxia, and recovery periods. Scalp Pot levels correlated well with carotid arterial levels while scalp Pcor, pH. and base deficit did not. Oxygen consumption paralleled Pot levels.
Methods
MEASUREMENT of blood gas and pH levels in capillary blood from the scalp as introduced by Saling* and Bretscher and SalingZ has achieved widespread use as a method of monitoring fetal well-being during labor. Only two reports of animal studies have been presented,3l 4 and neither of these analyzed oxygen consumption or blood flow data. This paper reports data comparing scalp pH, PO,, Pcoz, and base-deficit values in the fetal lamb to the same data in fetal carotid arterial and jugular venous blood and to cephalic blood flow, oxygen consumption, blood pressure, and heart rate during control and hypoxia periods. From the Department Gynecology, University College of Medicine.
of Obstetrics of Kentucky,
Supported by National Health Grant No. HE
Institutes 12476-02.
T.;;ived
for
publication
October
Twelve near-term pregnant ewes of mixed breed were used in this study. Each ewe was placed in the left lateral recumbent position, and catheters were inserted into the right jugular vein and carotid artery with 2 per cent lidocaine HCl local anesthesia. A tracheostomy was performed and attached to a Bird respirator. The ewe was given pentobarbital sodium anesthesia (average dose 15.2 mg. per kilogram) which was supplemented as necessary throughout the rest of the experiment. The uterus was exposed through a right paramedian infraumbilical incision, and the pregnant horn was marsupialized to the abdominal wound. The fetus was delivered, and the edges of the uterine incision were clamped to the fetal abdomen around the umbilicus to protect the umbilical cord. The fetal snout was covered with a saline-filled glove to prevent respiration. Both common
and
of 19, 397
398
Shier
and
February 1, 1972 Am. J. Obstet. Gynecol.
Dilts
carotid arteries were exposed and fitted with cuff-type electromagnetic flow transducers. Catheters were inserted in the left axillary artery and the left jugular vein via the temporal vein. The fetal scalp was shaved. The flow probes were connected to balanced field electromagnetic flowmeters. Fetal and maternal arterial pressures were measured with Sanborn pressure transducers. Pulsatile and electrically averaged pressure and flow signals were recorded on a HewlettPackard heated stylus rectilinear recorder at 5 minute intervals during the control and recovery periods and continuously during the period of hypoxia. A silicone jelly was applied to the scalp, and scalp blood samples were collected in 2 or 3 heparinized capillary tubes from a stab wound. The stab wound was made with a scalpel to a depth of 2 to 3 mm. Blood samples were collected anaerobically from
Table I. Maternal
blood
gas and acid-base
values Hypoxia+
Maternal arterial
of all data ?r 1 SE.
118.1 31.4 7.49 1.2
+ + t +
15 min. 21.8 + 1.2$ 22.6 + 0.3f 21.3 f. 0.2% 7.64 * O.Ol$ 7.61 t 0.012 -3.2 t 0.2$ -3.0 + 0.4 5 min.
Control”
PO* (mm. Hg) Pcoz (mm. Hg) PH Base deficit (mEq./L.) ‘Mean
the maternal carotid artery, fetal axillary artery and jugular vein, and fetal scalp 2 or 3 times each during the control and recovery periods and at 5 and 15 minutes during the period of hypoxia. One fetus died after 12 minutes of hypoxia. A blood sample taken at 11 minutes was grouped with the 15 minute samples from the other animals. There were only 11 animals in the recovery period when samples were collected at 5 and 20 minutes. These were analyzed immediately for PO*, PcoZ, and pH on an IL ultramicro Model 113 blood gas and pH analyzer. Base deficit was calculated on a Radiometer blood gas calculator-type BGCl, and the per cent of hemoglobin saturation by oxygen was estimated from published lamb hemoglobin oxygen dissociation curves.‘j Fetal arterial microhematocrit determinations were made once during each period. Following surgical preparation, a control
11.2 0.7 0.01 0.6
Recovery*
95.3 29.7 7.51 1.2
2 + + r
14.5 0.7 0.02 0.9
of mean.
tMean + 1 S.E. of diierence. $P < 0.005.
Table II. Maternal
and fetal
hemodynamics Minutes
121.1 + 1.0
2 127.1 2 0.5
4 130.0$ i: 0.7
6 130.1$ + 0.5
8 128.6$ i: 0.7
119.2 t 1.0
125.03 + 0.9
137.3$ f: 1.0
143.62 + 0.9
145.5$ + 1.3
58.3 t 0.4
57.42 ?r 0.2
59.2 + 0.5
60.9 + 0.6
66.3s c 0.7
201.0 + 1.9
210.8 i: 2.3
199.1 2 2.7
195.8 2 3.8
181.8 2 5.9
14.0 + 0.4
13.5 + 0.2
16.8% 2 0.4
17.4$ + 0.3
17.1$ A 0.4
Control*
Maternal arterial (mm. W Maternal
pressure
heart rate (per min.)
Fetal arterial pressure (mm. H.4 Fetal heart rate (per min.) Bilateral carotid flow (ml./Kg./min. g) *Mean
of all data ?. 1 S.E. of mean.
tMean 2 1 S.E. of difference. SP < 0.05. gPer kilogram of ferns.
of
Volume Number
112 3
Blood
period averaging 85 minutes was observed. Ninety-five per cent 0, and five per cent CO, mixed with room air were provided during the control and recovery periods. Hypoxia was induced by administering 6 per cent 0, and 94 per cent nitrogen. The hypoxia period averaged 18 minutes with a range of 11 to 23 minutes. A recovery period followed, averaging 68 minutes. Respiratory rate was not controlled in any of the periods. Results Maternal arterial blood gas and acid-base data are displayed in Table I. Arterial Paz and PcoB both decreased significantly during hypoxia. pH increased significantly, reflecting the drop in Pco, secondary to hyperventilation. Base deficit was more variable but decreased significantly by the second measurement during hypoxia. Maternal and fetal hemodynamic data are presented in Table II. Maternal arterial blood pressure and heart rate both increased during hypoxia, heart rate more so than blood pressure. Significance values are noted in Table II. Fetal arterial blood pressure decreased initially, then increased, but tended to decrease below control levels by the end of the hypoxia period. Four of the changes were statistically significant as noted. The fetal heart rate (Table II) rose at 2
gas
values
and
oxygen
consumption
399
minutes of hypoxia and then decreased throughout the period of hypoxia. However, none of these changes was statistically significant, even by analysis of paired differences. Bilateral carotid artery blood flow, after an initial drop, increased throughout the period of hypoxia with significance in 6 of the 10 measurements. Fetal cephalic blood flow and oxygen consumption (per kilogram of fetus) are presented in Table III. Oxygen consumption decreased initially (5 min.) during hypoxia but returned toward normal by mid-hypoxia (15 min.). The arteriovenous difference in oxygen content was significantly decreased at both sampling times. Carotid artery flow was increased but not significantly so at the times used for oxygen consumption calculation. Fetal PO, values are listed in Table IV. Paz decreased markedly and significantly during hypoxia from each site-carotid artery, jugular vein, and scalp. During the control period, scalp PO, correlated well with arterial blood values in 2 of the 3 samples and was close in the third. Scalp PO, was significantly different from venous levels at all 3 times. During hypoxia, scalp PO, values are not significantly different from either arterial or venous levels, though they are closer in value to arterial values than to venous levels. Note that arterial and venous levels are separated by less than 1.5 mm. Hg.
-...-~-- - .. --hypoxia+
-1 10
12
122.3 2 0.9
127.3
!: 0.6
t 2.0
148.32 + 1.6
66.7$ t 0.7
65.1s
+ 0.9
181.8 + 5.9
20.74 t 0.6
146.4$
I
16
18
20
124.5
127.3$
117.1 +- 1.1
?r 0.8
+- 0.8
124.4 2 1.2
116.1
2 0.9 143.0$ + 2.1
136.3$ f 2.9
130.0
137.1$
119.7
t
5 3.3
+ 2.6
62.4 2 0.9
58.8
56.5
57.0
+ 1.0
+ 1.4
2 0.9
185.0 f. 7.6
182.5 k 6.7
170.0 + 6.4
178.6 + 3.7
197.5
+ 2.4
+ 5.5 20.6$ 2 0.7
17.2
16.5 2 1.4
17.6 + 1.4
13.5
t 0.5
+ 0.7
177.5
14
19.0$
k 1.0
1 Recovery*
1.7
57.7 4 0.7
400
February 1, 1972 Am. J. Obstet. Gynecol.
Shier and Dilts
Table
III.
Fetal cephalic
blood
flow and oxygen
1 Oxygen
consumption
Control”
5 min.
HyP;riai
Recovery”
15 min.
0.32
I! 0.02
0.21
i: 0.018
0.29 + 0.02
0.27
2 0.03
2.6
?r 0.2
1.6
+ 0.1s
1.9
2.2
2 0.2
12.3
2 0.4
+ 0.5
consumption
(ml./Kg./min.$‘) Arteriovenous (ml./100
difference
0,
5 0.1s
ml.)
Bilateral carotid (ml./Kg./min.$)
flow
“Mean
of all data + 1 S.E. of mean.
tMean
A 1 S.E. of difference.
$Per kiIogram
13.1
t
0.4
15.3
? 0.7
12.3
P*
5 min.
of fetus.
8P < 0.025.
Table IV. Fetal
PO, values
(mm.
Hg)
controz 20
Arterial >
W
Scalp pt = Significance = Significance
40
20.8 0.05
min.
21.1 > 0.05 20.3 < 0.005
19.3 <
Venous ‘P tP
min.
0.01
14.7
Hypoxia 60
21.7 < 0.05 19.0 < 0.025
14.6
of difference of difference
15.6
of adjacent of sampling
Table V. Fetal Pco2 values
(mm.
min.
P* <
Arterial pt scalp
pt
Venous *P = Significance ?P
=
Significance
< 0.005 41.9 > 0.05 38.2 of difference
7.2 0.05 I%5
<
>
0.01
<
0.025
5.8
<
0.025
> < 0.025
0.01
> 7:9
18.7 < 0.025 15.4 > 0.05 14.6
min.
21.2 0.05 19.8 > 0.05 15.9 >
Hg) Hypoxia 60
36.5 0.05 41.1 > 0.05 39.6
40.8 0.05 44.4 > 0.05 40.4
P*
min.
< 0.005
5 min.
15
min.
1 20
min.
< 0.025
P+
5 min.
( 20 min.
7.34 < 0.025 7.32 > 0.05 7.32
7.36 > 0.05 7.35 > 0.05 7.34
5 min.
( 15 min.
7.44 ;,;;5
7.45 < 0.005 7.37 > 0.05 7.38
<
0.005
5 min. 37.9 0.05 39.2 > 0.05 38.4
P*
> 0.05
P*
31.4 <0.005 39.6 < 0.05 36.1
0.0’5
<
<
Recovery
32.1 0.005 40.4 < 0.025 36.5
>
of adjacent
of difference
8.8 0.05 25
1 20
test periods. sites.
40 min. <
min.
0.005
Control
20 min. 36.1
15
> <
Recovery
5 min.
37.9 < 0.05 42.2 > 0.05 38.4
>
> 0.05
test periods.
of sampling
sites.
Table VI. Fetal pH values Control 20
Arterial pt
Scalp pt
Venous *P = Significance tP
=
Significance
min.
[ 40
7.36 > 0.05 7.34 > 0.05 7.34 of difference of difference
min.
7.37 > 0.05 7.36 > 0.05 7.34 of adjacent
Hypoxia 1 60
min.
7.39 > 0.05 7.36 > 0.05 7.37
<
0.025 <
< <
0.05 0.05
> 0:05 7.38
Recovery
<
0.025
<
0.05
<
0.05
test periods.
of sampling
sites.
Recovery values are similar to control levels. Table V presents fetal Pco, data. There is a significant drop in arterial and venous Pco, during hypoxia but not in scalp levels. At all measuring points, scalp Pcoz levels are higher than either arterial or venous
levels. Scalp values are best correlated with venous Pcoz levels in the control and recovery periods and with neither during the hypoxia period. Fetal pH values are presented in Table VI. A significant increase in pH occurred
Volume Number
112 3
Blood gas values
Table VII. Fetal base-deficit 20 Arterial ‘Pt Scalp ‘Pt Venous
E5
=
Table VIII.
65
iii25 4.2
Experiment
15 min.
:::5
1.9 > 0.05 2.6 > 0.05 3.0
> <
0.01
>
0.3 0.02.5 2.7
< 3.6
of adjacent
of difference
Recovery --
5 min.
< 0.05
;::5
<
of difference
P*
>
4.7
Significance
1 60 min.
EL
20::5
401
(mEq./L.)
>
>
consumption
Hypoxia
Control 1 40 min.
min.
>
*P = Significance tP
values
and oxygen
<
0.05
P* <
5 min.
0.05
20
:::5
3.4 ;> 0.03 II.? < 0.05 4.5
> <
0.01
6.0 0.05 6.8
> < 0.05
min.
test periods.
of sampling
sites.
No. 9 --_ .-__ Heart rate (beats/ min.)
Arterial pressure (mm. Hz) 55 + 1
Controlt Minutes
-I 5
221
Art&o-
Right carotid flow (ml/Kg./ min.*) 5.1
Left carotid flow (ml./Kg./ min.“)
t
0.2
8.4
t
I
Total carotid pow (ml./Kg./ min.*)
diflerence (ml./100 ml.)
Oxygen consumption (ml./Kg./ min.*)
13.5
2.5
0.32
0.6
2 0.5
Ul?TIOUS
2 0.1
t
0.02
of hypoxia
1 3 5 7 9 11 13
55 55 55 57 65 72 60
Recovery? ‘Per
59 kilogram
240 250 220 160 150 130 60
t
2
183
2 5
4.8 5.1 6.2 7.5 8.9 9.6 6.9 4.8
5.6 6.8 8.0 8.8 12.8 12.0 13.5
+ 0.5
7.5
10.4 11.9 14.2 16.3 21.7 21.6 ‘0.4
rf: 1.0
12.3
t
1.5
1.6
0.22
1.4
0.70
1.8
t
0.4
0.28
” 0.01
of fetus.
t i 1 SE.
Table IX. Experiment
No. 9 .___ Pot
A* Control
)
(mm.
ffd
St
1
PC08 (mm. Hd (
S
Base deficit (mEq./L. j
PH
V$
A
1
V
14.5 15.5 13.5
34.5 34 37
41 39 40
47 36 36.5
7.45 7.47 7.50
22.5 23.5 23
13 23 22
Hypoxia
10 6
10 6.5
8 4.5
29 28
35.5 37.5
37.5 35
Recovery
17 23
14.5 20
13.5 15
36 30
33.5 38
37.5
-A
1
S
j
V
A
7.45 7.44
7.38 7.37 7.44
-0.4 -1.3 -5.1
/
-2.8 -‘J, 7
S
!
-3.0 4.0 -0.6
7.50 7.56
7.52 7.49
7.50 7.52
-0.6 -3.7
-6.0 -5.0
-5..3 -5.7
7.45 7.49
7.46 7.45
7.44 7.44
-1.2 --0.6
-0.7 -2.3
-_
J’
--I.4
*Arterial. 1Scalp. $VWXls.
at all 3 sampling sites during hypoxia. Scalp pH is best correlated with venous pH although during the control period the difference between arterial and venous pH is small enough that scalp pH correlates with both. Table VII presents fetal base-deficit data. Scalp values correlate poorly with both arterial and venous values although all three drop significantly during hypoxia.
Tables VIII and IX display a typical experiment, No. 9. Profound bradycardia developed near the conclusion of the hypoxia period. Comment
This experimental design has been used previously in studies of hypoxia.?+ Significant levels of hypoxia were obtained as noted by
402
Shier
and
Dilts
the changes in maternal and fetal PoB values (Tables I and IV). The fetal arterial catheter was placed in the left axillary artery and advanced into the subclavian artery. Care was taken not to advance the catheter to or beyond the origin of the left carotid artery since a marked decrease in carotid artery flow occurred when this was done. The jugular vein catheter was placed in the temporal vein and advanced into the jugular in order not to disturb or occlude cephalic venous drainage through the jugular vein. A silicone jelly was applied to the scalp to make the bIood bead for easier collection in micro-capillary tubes. In spite of this, it was difficult to collect many of the samples, and air bubbles and clots within the tubes were frequent. When this occurred, pH could not be determined with the IL micro apparatus. Also, hematoma formation was common. No major hemorrhage occurred into a hematoma, but finding a new site for scalp puncture and collection was difficult. The fetal scalp was under direct vision and observation during these experiments SO that pressure could be applied to the stab wounds to prevent a major hemorrhage. Circulating Pcoz values are reported to be the primary control mechanism for carotid artery blood flow, with a direct relationship between the two.lO-l” PO? levels are less effective until severe hypoxia is reached. In this series of experiments, the levels of hypoxia reached were low enough to cause a significant rise in bilateral carotid artery flow independent of PcoZ. Because of the rise in flow, the marked fall in Paz levels and consequent decrease in arteriovenous difference in oxygen content were counteracted after an initial decrease in oxygen consumption occurred. Oxygen consumption at middle to late hypoxia was the same as during the control period.*O Hypoxia is reported to cause a decrease in fetal effective cardiac output (ascending aorta flow plus ductus arteriosus flow) and in umbilical flo~.‘-~ Rough calculation from the data in Table II shows a decrease in resistance in the cerebral circulation through-
February 1, 1972 Am. J. Obstet. Gynecol.
out the period of hypoxia. This does not prove active vasodilatation but is suggestive of it since cardiac output is decreased. Calculated resistance in the umbilical circulation is increased during hypoxia. It is, of course, possible that this circuit (umbilical) is the major control center and that flow and pressure changes in the head are passive and dependent on the umbilical circulation. Investigation of the 2 circuits jointly will be necessary, probably with isolation of one or both. A typical experiment is displayed in Tables VIII and IX. Blood flow did rise markedly, and oxygen consumption was only transiently lowered during hypoxia, in spite of a moderate to marked decrease in arteriovenous difference in oxygen content. The head was definitely protected during this period of hypoxia. Also, there was a period of fetal tachycardia followed by severe bradycardia which must be significant but does not show as such when data for each period are grouped or by analysis of paired differences. There also was a slight rise in fetal arterial pressure during hypoxia. This pattern is typical of most of the experiments-tachycardia and hypertension followed by profound bradycardia as the period of hypoxia lengthened. Scalp blood data are displayed in Tables IV through VII. Measurements of scalp Pop are very close to carotid arterial Paz levels in the control and recovery periods. During hypoxia, the difference between arterial and venous levels was so small ( 1.5 mm. Hg) that scalp levels correlated with both, although closer to arterial levels. This indicates that the sampling method obtained arterial rather than venous blood. Scalp Pco, levels do not realistically correlate with either arterial or venous levels and are consistently higher than either. No explanation for this is readily apparent. Systematic error in analysis or sampIe collection may be involved. It is also possible that these Pco, values are real and peculiar to the scalp. In any event, this discrepancy casts some doubt on all the blood gas and pH data from the scalp until the data are duplicated in another series of experiments. Scalp Pco,
Volume Number
112 3
in these experiments cannot be said to be representative of cerebral PcoZ. Scalp pH correlates well with jugular venous pH levels. During hypoxia, the difference between arterial and venous pH levels increases. This must reflect the increased hydrogen ion release or acidosis expected during hypoxia. The marked rise in pH in both mother and fetus during hypoxia is associated with maternal hyperventilation and a significant decrease in maternal and fetal Pco, levels. Base-deficit levels from scalp blood are not representative of either arterial or venous blood. This is expected since PcoZ and pH data are used in the calculation of base deficit. Previous animal studies in the lamb3 and monkey4 found better correlation between scalp capillary and carotid arterial blood values than are reported here. However, there is enough difference in the experimental design utilized and in the extent of surgical dissection used in the present studies to make comparison difficult. As would be
Blood gas values
and oxygen
consumption
403
expected, changes in oxygen consumption correspond to the changes noted in scalp, carotid, and jugular blood PoB levels. In Experiment No. 9 (Table IX), only the scalp PO? data were consistently representative of either arterial or venous blood. However, even here there was no way to predict whether the scalp sample was closer to arterial or to venous levels. A large change in PO, levels may mean only that the sample being studied is more similar to arterial than to venous levels, as in the first 2 scalp PO, results, 13 and 23. Without concomitant measurement of carotid artery and jugular vein Po?‘s, this change could easily be mistaken to indicate fetal hypoxia, especially if it were the other direction. This experimental protocol was not designed to answer clinical questions concerning the reliability of scalp sampling in assessing fetal well-being during labor. The effects of head compression and scalp edema are unknown. New experiments in monkeys may be able to answer some of the questions raised.
REFERENCES
1. 2. 3.
4.
5.
6.
Saling, E. : Z. Geburtshilfe Gynaekol. 161: 262, 1963. Bretscher, J., and Saling, E.: AM. J. OBSTET. GYNECOL. 97: 906. 1967. Gare, D. J., Whetham, J. C. G., and Henry, J. D.: AM. J. OBSTET. GYNECOL. 99: 722, 1967. Adamsons, K., Beard, R. W., and Myers, R. E.: AM. J. QBSTET. GYNECOL. 107: 435, 1970. Westersten, A., Rice, E., Brinkman, C. R., and Assali, N. S.: J. Appl. Physiol. 26: 497, 1969. Kirschbaum, T. H., DeHaven, J. C., Shapiro, N., and Assali, N. S.: AM. J. OBSTET. GYNECOL. 96: 741, 1966.
7.
8.-.
9.
10. 11. 12.
Brinkman, and Assali, 1970. Brinkman, baum, T.
C. R., III, Kirschbaum, N. S.: Gynecol. Invest. C. II.,
T. H., 1: 115,
R., III, Weston, P., Kirschand Assali, N. S.: AM. J. OBSTET. GYNECOL. 108: 288, 1970. Dilts, P. V., Jr., Brinkman, C. R., III, Kirschbaum, T. H., and Assali, N. S.: AM. J. OBSTET. GYNECOL. 103: 138, 1969. Lucas, W., Kirschbaum, T., and Assali, N. S.: Am. J. Physiol. 210: 287, 1966. Purves, M. J., and James, I. M.: Circ. Res. 25: 651, 1969. Quilligan, E. J., Dunnihoo, D. R., and Anderson, G. G.: A&f. J. OBSTET. GYNECOI.. 109: 706, 1971.
Comparison of fetal scalp, carotid, and jugular blood gas values and oxygen consumption in the lamb R.
W.
P.
V.
SHIER, DILTS,
Lexington,
M.D. JR.,
M.D.
Kentucky
Scalp pH, PO*, Pcog, and base-deficit values in the fetal lamb are cornbared to the same values in fetal carotid arterial and jugular venous blood and to fetal cephalic blood flow, oxygen consumption, blood pressure, and heart rate during control, hypoxia, and recovery periods. Scalp Pot levels correlated well with carotid arterial levels while scalp Pcor, pH. and base deficit did not. Oxygen consumption paralleled Pot levels.
Methods
MEASUREMENT of blood gas and pH levels in capillary blood from the scalp as introduced by Saling* and Bretscher and SalingZ has achieved widespread use as a method of monitoring fetal well-being during labor. Only two reports of animal studies have been presented,3l 4 and neither of these analyzed oxygen consumption or blood flow data. This paper reports data comparing scalp pH, PO,, Pcoz, and base-deficit values in the fetal lamb to the same data in fetal carotid arterial and jugular venous blood and to cephalic blood flow, oxygen consumption, blood pressure, and heart rate during control and hypoxia periods. From the Department Gynecology, University College of Medicine.
of Obstetrics of Kentucky,
Supported by National Health Grant No. HE
Institutes 12476-02.
T.;;ived
for
publication
October
Twelve near-term pregnant ewes of mixed breed were used in this study. Each ewe was placed in the left lateral recumbent position, and catheters were inserted into the right jugular vein and carotid artery with 2 per cent lidocaine HCl local anesthesia. A tracheostomy was performed and attached to a Bird respirator. The ewe was given pentobarbital sodium anesthesia (average dose 15.2 mg. per kilogram) which was supplemented as necessary throughout the rest of the experiment. The uterus was exposed through a right paramedian infraumbilical incision, and the pregnant horn was marsupialized to the abdominal wound. The fetus was delivered, and the edges of the uterine incision were clamped to the fetal abdomen around the umbilicus to protect the umbilical cord. The fetal snout was covered with a saline-filled glove to prevent respiration. Both common
and
of 19, 397
398
Shier
and
February 1, 1972 Am. J. Obstet. Gynecol.
Dilts
carotid arteries were exposed and fitted with cuff-type electromagnetic flow transducers. Catheters were inserted in the left axillary artery and the left jugular vein via the temporal vein. The fetal scalp was shaved. The flow probes were connected to balanced field electromagnetic flowmeters. Fetal and maternal arterial pressures were measured with Sanborn pressure transducers. Pulsatile and electrically averaged pressure and flow signals were recorded on a HewlettPackard heated stylus rectilinear recorder at 5 minute intervals during the control and recovery periods and continuously during the period of hypoxia. A silicone jelly was applied to the scalp, and scalp blood samples were collected in 2 or 3 heparinized capillary tubes from a stab wound. The stab wound was made with a scalpel to a depth of 2 to 3 mm. Blood samples were collected anaerobically from
Table I. Maternal
blood
gas and acid-base
values Hypoxia+
Maternal arterial
of all data ?r 1 SE.
118.1 31.4 7.49 1.2
+ + t +
15 min. 21.8 + 1.2$ 22.6 + 0.3f 21.3 f. 0.2% 7.64 * O.Ol$ 7.61 t 0.012 -3.2 t 0.2$ -3.0 + 0.4 5 min.
Control”
PO* (mm. Hg) Pcoz (mm. Hg) PH Base deficit (mEq./L.) ‘Mean
the maternal carotid artery, fetal axillary artery and jugular vein, and fetal scalp 2 or 3 times each during the control and recovery periods and at 5 and 15 minutes during the period of hypoxia. One fetus died after 12 minutes of hypoxia. A blood sample taken at 11 minutes was grouped with the 15 minute samples from the other animals. There were only 11 animals in the recovery period when samples were collected at 5 and 20 minutes. These were analyzed immediately for PO*, PcoZ, and pH on an IL ultramicro Model 113 blood gas and pH analyzer. Base deficit was calculated on a Radiometer blood gas calculator-type BGCl, and the per cent of hemoglobin saturation by oxygen was estimated from published lamb hemoglobin oxygen dissociation curves.‘j Fetal arterial microhematocrit determinations were made once during each period. Following surgical preparation, a control
11.2 0.7 0.01 0.6
Recovery*
95.3 29.7 7.51 1.2
2 + + r
14.5 0.7 0.02 0.9
of mean.
tMean + 1 S.E. of diierence. $P < 0.005.
Table II. Maternal
and fetal
hemodynamics Minutes
121.1 + 1.0
2 127.1 2 0.5
4 130.0$ i: 0.7
6 130.1$ + 0.5
8 128.6$ i: 0.7
119.2 t 1.0
125.03 + 0.9
137.3$ f: 1.0
143.62 + 0.9
145.5$ + 1.3
58.3 t 0.4
57.42 ?r 0.2
59.2 + 0.5
60.9 + 0.6
66.3s c 0.7
201.0 + 1.9
210.8 i: 2.3
199.1 2 2.7
195.8 2 3.8
181.8 2 5.9
14.0 + 0.4
13.5 + 0.2
16.8% 2 0.4
17.4$ + 0.3
17.1$ A 0.4
Control*
Maternal arterial (mm. W Maternal
pressure
heart rate (per min.)
Fetal arterial pressure (mm. H.4 Fetal heart rate (per min.) Bilateral carotid flow (ml./Kg./min. g) *Mean
of all data ?. 1 S.E. of mean.
tMean 2 1 S.E. of difference. SP < 0.05. gPer kilogram of ferns.
of
Volume Number
112 3
Blood
period averaging 85 minutes was observed. Ninety-five per cent 0, and five per cent CO, mixed with room air were provided during the control and recovery periods. Hypoxia was induced by administering 6 per cent 0, and 94 per cent nitrogen. The hypoxia period averaged 18 minutes with a range of 11 to 23 minutes. A recovery period followed, averaging 68 minutes. Respiratory rate was not controlled in any of the periods. Results Maternal arterial blood gas and acid-base data are displayed in Table I. Arterial Paz and PcoB both decreased significantly during hypoxia. pH increased significantly, reflecting the drop in Pco, secondary to hyperventilation. Base deficit was more variable but decreased significantly by the second measurement during hypoxia. Maternal and fetal hemodynamic data are presented in Table II. Maternal arterial blood pressure and heart rate both increased during hypoxia, heart rate more so than blood pressure. Significance values are noted in Table II. Fetal arterial blood pressure decreased initially, then increased, but tended to decrease below control levels by the end of the hypoxia period. Four of the changes were statistically significant as noted. The fetal heart rate (Table II) rose at 2
gas
values
and
oxygen
consumption
399
minutes of hypoxia and then decreased throughout the period of hypoxia. However, none of these changes was statistically significant, even by analysis of paired differences. Bilateral carotid artery blood flow, after an initial drop, increased throughout the period of hypoxia with significance in 6 of the 10 measurements. Fetal cephalic blood flow and oxygen consumption (per kilogram of fetus) are presented in Table III. Oxygen consumption decreased initially (5 min.) during hypoxia but returned toward normal by mid-hypoxia (15 min.). The arteriovenous difference in oxygen content was significantly decreased at both sampling times. Carotid artery flow was increased but not significantly so at the times used for oxygen consumption calculation. Fetal PO, values are listed in Table IV. Paz decreased markedly and significantly during hypoxia from each site-carotid artery, jugular vein, and scalp. During the control period, scalp PO, correlated well with arterial blood values in 2 of the 3 samples and was close in the third. Scalp PO, was significantly different from venous levels at all 3 times. During hypoxia, scalp PO, values are not significantly different from either arterial or venous levels, though they are closer in value to arterial values than to venous levels. Note that arterial and venous levels are separated by less than 1.5 mm. Hg.
-...-~-- - .. --hypoxia+
-1 10
12
122.3 2 0.9
127.3
!: 0.6
t 2.0
148.32 + 1.6
66.7$ t 0.7
65.1s
+ 0.9
181.8 + 5.9
20.74 t 0.6
146.4$
I
16
18
20
124.5
127.3$
117.1 +- 1.1
?r 0.8
+- 0.8
124.4 2 1.2
116.1
2 0.9 143.0$ + 2.1
136.3$ f 2.9
130.0
137.1$
119.7
t
5 3.3
+ 2.6
62.4 2 0.9
58.8
56.5
57.0
+ 1.0
+ 1.4
2 0.9
185.0 f. 7.6
182.5 k 6.7
170.0 + 6.4
178.6 + 3.7
197.5
+ 2.4
+ 5.5 20.6$ 2 0.7
17.2
16.5 2 1.4
17.6 + 1.4
13.5
t 0.5
+ 0.7
177.5
14
19.0$
k 1.0
1 Recovery*
1.7
57.7 4 0.7
400
February 1, 1972 Am. J. Obstet. Gynecol.
Shier and Dilts
Table
III.
Fetal cephalic
blood
flow and oxygen
1 Oxygen
consumption
Control”
5 min.
HyP;riai
Recovery”
15 min.
0.32
I! 0.02
0.21
i: 0.018
0.29 + 0.02
0.27
2 0.03
2.6
?r 0.2
1.6
+ 0.1s
1.9
2.2
2 0.2
12.3
2 0.4
+ 0.5
consumption
(ml./Kg./min.$‘) Arteriovenous (ml./100
difference
0,
5 0.1s
ml.)
Bilateral carotid (ml./Kg./min.$)
flow
“Mean
of all data + 1 S.E. of mean.
tMean
A 1 S.E. of difference.
$Per kiIogram
13.1
t
0.4
15.3
? 0.7
12.3
P*
5 min.
of fetus.
8P < 0.025.
Table IV. Fetal
PO, values
(mm.
Hg)
controz 20
Arterial >
W
Scalp pt = Significance = Significance
40
20.8 0.05
min.
21.1 > 0.05 20.3 < 0.005
19.3 <
Venous ‘P tP
min.
0.01
14.7
Hypoxia 60
21.7 < 0.05 19.0 < 0.025
14.6
of difference of difference
15.6
of adjacent of sampling
Table V. Fetal Pco2 values
(mm.
min.
P* <
Arterial pt scalp
pt
Venous *P = Significance ?P
=
Significance
< 0.005 41.9 > 0.05 38.2 of difference
7.2 0.05 I%5
<
>
0.01
<
0.025
5.8
<
0.025
> < 0.025
0.01
> 7:9
18.7 < 0.025 15.4 > 0.05 14.6
min.
21.2 0.05 19.8 > 0.05 15.9 >
Hg) Hypoxia 60
36.5 0.05 41.1 > 0.05 39.6
40.8 0.05 44.4 > 0.05 40.4
P*
min.
< 0.005
5 min.
15
min.
1 20
min.
< 0.025
P+
5 min.
( 20 min.
7.34 < 0.025 7.32 > 0.05 7.32
7.36 > 0.05 7.35 > 0.05 7.34
5 min.
( 15 min.
7.44 ;,;;5
7.45 < 0.005 7.37 > 0.05 7.38
<
0.005
5 min. 37.9 0.05 39.2 > 0.05 38.4
P*
> 0.05
P*
31.4 <0.005 39.6 < 0.05 36.1
0.0’5
<
<
Recovery
32.1 0.005 40.4 < 0.025 36.5
>
of adjacent
of difference
8.8 0.05 25
1 20
test periods. sites.
40 min. <
min.
0.005
Control
20 min. 36.1
15
> <
Recovery
5 min.
37.9 < 0.05 42.2 > 0.05 38.4
>
> 0.05
test periods.
of sampling
sites.
Table VI. Fetal pH values Control 20
Arterial pt
Scalp pt
Venous *P = Significance tP
=
Significance
min.
[ 40
7.36 > 0.05 7.34 > 0.05 7.34 of difference of difference
min.
7.37 > 0.05 7.36 > 0.05 7.34 of adjacent
Hypoxia 1 60
min.
7.39 > 0.05 7.36 > 0.05 7.37
<
0.025 <
< <
0.05 0.05
> 0:05 7.38
Recovery
<
0.025
<
0.05
<
0.05
test periods.
of sampling
sites.
Recovery values are similar to control levels. Table V presents fetal Pco, data. There is a significant drop in arterial and venous Pco, during hypoxia but not in scalp levels. At all measuring points, scalp Pcoz levels are higher than either arterial or venous
levels. Scalp values are best correlated with venous Pcoz levels in the control and recovery periods and with neither during the hypoxia period. Fetal pH values are presented in Table VI. A significant increase in pH occurred
Volume Number
112 3
Blood gas values
Table VII. Fetal base-deficit 20 Arterial ‘Pt Scalp ‘Pt Venous
E5
=
Table VIII.
65
iii25 4.2
Experiment
15 min.
:::5
1.9 > 0.05 2.6 > 0.05 3.0
> <
0.01
>
0.3 0.02.5 2.7
< 3.6
of adjacent
of difference
Recovery --
5 min.
< 0.05
;::5
<
of difference
P*
>
4.7
Significance
1 60 min.
EL
20::5
401
(mEq./L.)
>
>
consumption
Hypoxia
Control 1 40 min.
min.
>
*P = Significance tP
values
and oxygen
<
0.05
P* <
5 min.
0.05
20
:::5
3.4 ;> 0.03 II.? < 0.05 4.5
> <
0.01
6.0 0.05 6.8
> < 0.05
min.
test periods.
of sampling
sites.
No. 9 --_ .-__ Heart rate (beats/ min.)
Arterial pressure (mm. Hz) 55 + 1
Controlt Minutes
-I 5
221
Art&o-
Right carotid flow (ml/Kg./ min.*) 5.1
Left carotid flow (ml./Kg./ min.“)
t
0.2
8.4
t
I
Total carotid pow (ml./Kg./ min.*)
diflerence (ml./100 ml.)
Oxygen consumption (ml./Kg./ min.*)
13.5
2.5
0.32
0.6
2 0.5
Ul?TIOUS
2 0.1
t
0.02
of hypoxia
1 3 5 7 9 11 13
55 55 55 57 65 72 60
Recovery? ‘Per
59 kilogram
240 250 220 160 150 130 60
t
2
183
2 5
4.8 5.1 6.2 7.5 8.9 9.6 6.9 4.8
5.6 6.8 8.0 8.8 12.8 12.0 13.5
+ 0.5
7.5
10.4 11.9 14.2 16.3 21.7 21.6 ‘0.4
rf: 1.0
12.3
t
1.5
1.6
0.22
1.4
0.70
1.8
t
0.4
0.28
” 0.01
of fetus.
t i 1 SE.
Table IX. Experiment
No. 9 .___ Pot
A* Control
)
(mm.
ffd
St
1
PC08 (mm. Hd (
S
Base deficit (mEq./L. j
PH
V$
A
1
V
14.5 15.5 13.5
34.5 34 37
41 39 40
47 36 36.5
7.45 7.47 7.50
22.5 23.5 23
13 23 22
Hypoxia
10 6
10 6.5
8 4.5
29 28
35.5 37.5
37.5 35
Recovery
17 23
14.5 20
13.5 15
36 30
33.5 38
37.5
-A
1
S
j
V
A
7.45 7.44
7.38 7.37 7.44
-0.4 -1.3 -5.1
/
-2.8 -‘J, 7
S
!
-3.0 4.0 -0.6
7.50 7.56
7.52 7.49
7.50 7.52
-0.6 -3.7
-6.0 -5.0
-5..3 -5.7
7.45 7.49
7.46 7.45
7.44 7.44
-1.2 --0.6
-0.7 -2.3
-_
J’
--I.4
*Arterial. 1Scalp. $VWXls.
at all 3 sampling sites during hypoxia. Scalp pH is best correlated with venous pH although during the control period the difference between arterial and venous pH is small enough that scalp pH correlates with both. Table VII presents fetal base-deficit data. Scalp values correlate poorly with both arterial and venous values although all three drop significantly during hypoxia.
Tables VIII and IX display a typical experiment, No. 9. Profound bradycardia developed near the conclusion of the hypoxia period. Comment
This experimental design has been used previously in studies of hypoxia.?+ Significant levels of hypoxia were obtained as noted by
402
Shier
and
Dilts
the changes in maternal and fetal PoB values (Tables I and IV). The fetal arterial catheter was placed in the left axillary artery and advanced into the subclavian artery. Care was taken not to advance the catheter to or beyond the origin of the left carotid artery since a marked decrease in carotid artery flow occurred when this was done. The jugular vein catheter was placed in the temporal vein and advanced into the jugular in order not to disturb or occlude cephalic venous drainage through the jugular vein. A silicone jelly was applied to the scalp to make the bIood bead for easier collection in micro-capillary tubes. In spite of this, it was difficult to collect many of the samples, and air bubbles and clots within the tubes were frequent. When this occurred, pH could not be determined with the IL micro apparatus. Also, hematoma formation was common. No major hemorrhage occurred into a hematoma, but finding a new site for scalp puncture and collection was difficult. The fetal scalp was under direct vision and observation during these experiments SO that pressure could be applied to the stab wounds to prevent a major hemorrhage. Circulating Pcoz values are reported to be the primary control mechanism for carotid artery blood flow, with a direct relationship between the two.lO-l” PO? levels are less effective until severe hypoxia is reached. In this series of experiments, the levels of hypoxia reached were low enough to cause a significant rise in bilateral carotid artery flow independent of PcoZ. Because of the rise in flow, the marked fall in Paz levels and consequent decrease in arteriovenous difference in oxygen content were counteracted after an initial decrease in oxygen consumption occurred. Oxygen consumption at middle to late hypoxia was the same as during the control period.*O Hypoxia is reported to cause a decrease in fetal effective cardiac output (ascending aorta flow plus ductus arteriosus flow) and in umbilical flo~.‘-~ Rough calculation from the data in Table II shows a decrease in resistance in the cerebral circulation through-
February 1, 1972 Am. J. Obstet. Gynecol.
out the period of hypoxia. This does not prove active vasodilatation but is suggestive of it since cardiac output is decreased. Calculated resistance in the umbilical circulation is increased during hypoxia. It is, of course, possible that this circuit (umbilical) is the major control center and that flow and pressure changes in the head are passive and dependent on the umbilical circulation. Investigation of the 2 circuits jointly will be necessary, probably with isolation of one or both. A typical experiment is displayed in Tables VIII and IX. Blood flow did rise markedly, and oxygen consumption was only transiently lowered during hypoxia, in spite of a moderate to marked decrease in arteriovenous difference in oxygen content. The head was definitely protected during this period of hypoxia. Also, there was a period of fetal tachycardia followed by severe bradycardia which must be significant but does not show as such when data for each period are grouped or by analysis of paired differences. There also was a slight rise in fetal arterial pressure during hypoxia. This pattern is typical of most of the experiments-tachycardia and hypertension followed by profound bradycardia as the period of hypoxia lengthened. Scalp blood data are displayed in Tables IV through VII. Measurements of scalp Pop are very close to carotid arterial Paz levels in the control and recovery periods. During hypoxia, the difference between arterial and venous levels was so small ( 1.5 mm. Hg) that scalp levels correlated with both, although closer to arterial levels. This indicates that the sampling method obtained arterial rather than venous blood. Scalp Pco, levels do not realistically correlate with either arterial or venous levels and are consistently higher than either. No explanation for this is readily apparent. Systematic error in analysis or sampIe collection may be involved. It is also possible that these Pco, values are real and peculiar to the scalp. In any event, this discrepancy casts some doubt on all the blood gas and pH data from the scalp until the data are duplicated in another series of experiments. Scalp Pco,
Volume Number
112 3
in these experiments cannot be said to be representative of cerebral PcoZ. Scalp pH correlates well with jugular venous pH levels. During hypoxia, the difference between arterial and venous pH levels increases. This must reflect the increased hydrogen ion release or acidosis expected during hypoxia. The marked rise in pH in both mother and fetus during hypoxia is associated with maternal hyperventilation and a significant decrease in maternal and fetal Pco, levels. Base-deficit levels from scalp blood are not representative of either arterial or venous blood. This is expected since PcoZ and pH data are used in the calculation of base deficit. Previous animal studies in the lamb3 and monkey4 found better correlation between scalp capillary and carotid arterial blood values than are reported here. However, there is enough difference in the experimental design utilized and in the extent of surgical dissection used in the present studies to make comparison difficult. As would be
Blood gas values
and oxygen
consumption
403
expected, changes in oxygen consumption correspond to the changes noted in scalp, carotid, and jugular blood PoB levels. In Experiment No. 9 (Table IX), only the scalp PO? data were consistently representative of either arterial or venous blood. However, even here there was no way to predict whether the scalp sample was closer to arterial or to venous levels. A large change in PO, levels may mean only that the sample being studied is more similar to arterial than to venous levels, as in the first 2 scalp PO, results, 13 and 23. Without concomitant measurement of carotid artery and jugular vein Po?‘s, this change could easily be mistaken to indicate fetal hypoxia, especially if it were the other direction. This experimental protocol was not designed to answer clinical questions concerning the reliability of scalp sampling in assessing fetal well-being during labor. The effects of head compression and scalp edema are unknown. New experiments in monkeys may be able to answer some of the questions raised.
REFERENCES
1. 2. 3.
4.
5.
6.
Saling, E. : Z. Geburtshilfe Gynaekol. 161: 262, 1963. Bretscher, J., and Saling, E.: AM. J. OBSTET. GYNECOL. 97: 906. 1967. Gare, D. J., Whetham, J. C. G., and Henry, J. D.: AM. J. OBSTET. GYNECOL. 99: 722, 1967. Adamsons, K., Beard, R. W., and Myers, R. E.: AM. J. QBSTET. GYNECOL. 107: 435, 1970. Westersten, A., Rice, E., Brinkman, C. R., and Assali, N. S.: J. Appl. Physiol. 26: 497, 1969. Kirschbaum, T. H., DeHaven, J. C., Shapiro, N., and Assali, N. S.: AM. J. OBSTET. GYNECOL. 96: 741, 1966.
7.
8.-.
9.
10. 11. 12.
Brinkman, and Assali, 1970. Brinkman, baum, T.
C. R., III, Kirschbaum, N. S.: Gynecol. Invest. C. II.,
T. H., 1: 115,
R., III, Weston, P., Kirschand Assali, N. S.: AM. J. OBSTET. GYNECOL. 108: 288, 1970. Dilts, P. V., Jr., Brinkman, C. R., III, Kirschbaum, T. H., and Assali, N. S.: AM. J. OBSTET. GYNECOL. 103: 138, 1969. Lucas, W., Kirschbaum, T., and Assali, N. S.: Am. J. Physiol. 210: 287, 1966. Purves, M. J., and James, I. M.: Circ. Res. 25: 651, 1969. Quilligan, E. J., Dunnihoo, D. R., and Anderson, G. G.: A&f. J. OBSTET. GYNECOI.. 109: 706, 1971.