Volume 153 Number 4

5. Hallman M, Kulovich M, Kirkpatrick E, Sugarman R, Gluck L. Phosphatidylinositol and phosphatidylglycerol in amniotic fluid: indices of lung maturity. AM J 0BSTET Gv­NECOL 1976; 125:613.

6. Morrison JC, Whybrew WD, Bucovaz ET, Wiser WL, Fish SA. The lecithin/sphingomyelin ratio in cases associated with fetomaternal disease. AM J OBSTET GYNECOL 1977; 127:363.

Lung profiles in isoimmunized pregnancy

7. Doran TA, Malone RM, Jones OV, Thompson DW, New ML. Amniotic fluid tests for fetal maturity in normal and abnormal pregnancies. AM J 0BSTET GYNECOL 1976; 125:586.

8. Quinlan KW, Buhi WC, Cruz AC. Fetal pulmonary ma­turity in isoimmunized pregnancies. AM J OBSTET GYNECOL

1984;148:787.

Electrical and mechanical uterine activity and gap junctions in peripartal sheep

A. Verhoeff, M.D., R. E. Garfield, Ph.D., J. Ramondt, M.D., and H. C. S. Wallenburg, M.D., Ph.D.

Rotterdam, The Netherlands, and Hamilton, Ontario, Canada

In 10 chronically instrumented pregnant ewes myometrial electrical activity and intrauterine pressure were measured and plasma levels of 17j3-estradiol and progesterone were determined in late pregnancy and

during and after labor. Myometrial biopsies were obtained to determine gap junction area. Plasma

progesterone levels fell 4 days before delivery, and 17[3-estradiol levels rose sharply 12 hours before delivery. Toward delivery the myometrial electrical pattern changed from infrequent bursts of long duration to frequent bursts of short duration, and the active pressure area of the intrauterine pressure cycles, the

apparent conduction velocity, and the rate of rise of intrauterine pressure cycles increased associated with

the changes in hormone levels. These changes were related to an increase in gap junction area. It is concluded that these results support the hypothesis that changes in concentrations of steroid hormones

lead to an increase in myometrial gap junction area, which improves the coordination of contractile activity of the uterus during labor. (AM J OBSTET GYNECOL 1985;153:447-54.)

Key words: Myometrial electrical activity, gap junctions, parturition

Labor in various species is preceded by or associated with hormonal changes, which proceed sequentially to achieve normal parturition. 1

·3 In sheep a decrease in

progesterone levels in plasma and uterine tissue, fol­lowed by an increase in estrogen and prostaglandins, is thought to lead to increased and coordinated con­tractility of the myometrium, which eventually results in delivery.'· 2 It has been proposed that the spread of electrical activity between muscle cells of the myome­trium, to synchronize their contractility during labor,

From the Department of Obstetrics and Gynecology, Medical School, Erasmus University, Rotterdam, and the Departments of Neuro­sciences and Obstetrics and Gynecology, McMaster University Health Sciences Centre, Hamilton.

This study was supported by a grant from the Medical Research Coun­cil of Canada and a grant from The Nether lands Organization for the Advancement of Pure Research.

Presented in part at the Thirtieth Annual Meeting of the Society for Gynecologic Investigation, Washington, D. C., March 17-20, 1983.

Reprint requests: H. C. S. Wallenburg, M.D., Ph.D., Department of Obstetrics and Gynecology, Erasmus University, Medical School, EE 2283, P. 0. Box 17 38, 3000 DR Rotterdam, The Netherlands.

may be facilitated by the development of gap junctions.4

Gap junctions are specialized cell-to-cell contacts that may provide sites of low resistance to the propagation of electrical signals between myometrial cells.4·6 The formation of gap junctions is accompanied by an aug­mentation of the electrical coupling between rat myo­metrial cells as measured in vitro.6 It has been shown that the area of gap junction contact between myo­metrial cells is small prior to labor, increases during labor, and declines shortly after delivery in rats,4· 5

• 7

rabbits, 8 sheep,9 and humans.'0 The results of various studies in rats5

• 7

• 11

• 12 and sheep9 indicate that the de­

velopment of gap junctions between myometrial cells may be modulated by changes in tissue levels of steroid hormones. However, the relationship between myo­metrial electrical and mechanical activity, changes in

steroid hormone levels, and the development of myo­metrial gap junctions before and during labor has not been investigated in vivo. The increase in myometrial effort that leads to delivery, in relation to gap junction formation, can only be investigated in vivo. In vitro

447

448 Verhoeff et al.

studies d.o not provide information on the activity of the entire myometrium and, in addition, the factors that control contractility in vivo may be altered in vitro.

Therefore, the present study was designed to com­pare myometrial activity, plasma levels of l 7p-estradiol and progesterone, and the number of myometrial gap junctions before, during, and after parturition in chronically instrumented ewes.

Material and methods

Studies were carried out m 10 chronically instru­mented unanesthetized pregnant ewes. Seven ewes had a single fetus and three ewes had a twin pregnancy. At 110 to 124 days' gestation operation was performed with the animal under general anesthesia with 500 mg of ketamine hydrochloride, 0.5 mg of atropine, and 300 to 500 mg of thiopental sodium administered in­travenously. The animals were intubated and ventilated with 40% oxygen, 60% nitrous oxide, and 0.5 to 4 vol% enflurane. A polyvinyl catheter was inserted into a fem­oral artery and advanced into the descending aorta. A lower midline laparotomy was performed and a preg­nant horn was exposed. For recording of electrical myo­metrial activity, three bipolar, silver chloride-coated, silver needle electrodes were fixed to the anterior part of the myometrium in the fundal, medial, and cervical regions of the pregnant horn. The needles of the elec­trodes were 3 mm long and had a diameter of 0.2 mm. The distance between electrodes (20 to 30 cm) was mea­sured. A sponge-tipped catheter was inserted into the amniotic cavity for recording of intrauterine pressure. The wires and catheters were passed subcutaneously to a pouch attached to the ewe's flank.

During the operation longitudinal strips of myo­metrium (5 by 2 by 0.1 cm) were taken from the fundal and medial regions of the pregnant horn for electron microscopy.

After a recovery period lasting at least 4 days, elec­trical and mechanical uterine activity was recorded daily for at least 2 hours, with the ewe in a quiet en­vironment. The electrical signals were filtered by a band-pass filter. For the lower and higher cutoff fre­quencies (- 3 dB) 1 and 30 Hz were selected. Intra­uterine pressure was measured by a Gould Statham P23 ID pressure transducer. The electrical myometrial ac­tivity signals from three different regions as well as the intrauterine pressure signal were recorded on a Gould Brush eight-channel polygraph with a paper speed of 25 mm · min - i and stored on magnetic tape.

Aortic blood samples were drawn for assay of the concentrations of progesterone and l 7p-estradiol at 4-day intervals from the fourth day after operation. When labor appeared to be imminent as judged from the electrical myometrial activity and intrauterine pres­sure signals, samples were drawn at 12-hour inter-

October 15, 1985 Am J Obstet Gynecol

vals. The samples were centrifuged immediately at 1380 x g for 10 minutes at 40° C; the plasma was stored at - 20° C until analysis.

Additional myometrial biopsies for electron micros­copy were obtained from the pregnant horn in three ewes before parturition, in eight animals during the second stage of labor, and in eight animals after par­turition. The procedure was performed with the ani­mals under epidural anesthesia with 6 to 10 ml of 5% bupivacaine after sedation with ketamine hydrochlo­ride. On these occasions the distance between the elec­trodes was again measured. The lambs were removed from the ewes after birth.

Analytic procedures. The electrical myometrial ac­tivity was analyzed visually for intermittent epochs of distinct electrical activity, referred to as bursts. Bursts were defined as episodes in which the amplitude of the electromyographic signals showed an increase to three times the baseline signal or more for longer than 15 seconds. Episodes occurring less than 15 seconds apart were taken as one burst. The bursts were analyzed for duration in minutes and frequency per hour. The ap­parent conduction velocity in cm · sec' was calculated by dividing the measured distance between the elec­trodes by the phase lag between the onset of bursts. The intrauterine pressure signals were analyzed for periodic elevations of intrauterine pressure of at least 3.5 mm Hg, with a return to baseline level; these are called intrauterine pressure cycles. The intrauterine pressure cycles were analyzed for duration in minutes and frequency per hour. The area of intrauterine pres­sure cycles, minus the basal tone (active pressure area) was measured by means of a digitizing tablet (Labo­ratory Computer System, Inc., Cambridge, Massachu­setts). Readily recognizable artifacts caused by bearing­down efforts of the ewe during labor were omitted. The areas were added during I-hour periods and ex­pressed in cm2 hr-' (1 cm2 = 500 mm Hg sec). The rate of rise of the intrauterine pressure cycles (mm Hg· sec') was calculated by dividing the maximum amplitude of the intrauterine pressure cycle by the time needed to reach it.

The methods for processing the tissue samples for electron microscopy and for quantitative determination of myometrial gap junctions have been published else­where.10· 11 Briefly, the length of the plasma mem­brane was determined in 20 electron micrographs (at x 33,600 magnification) from each tissue. Each possi­ble gap junction was further enlarged to x 100,000 magnification for identification and measurement. The area of gap junction membrane relative to the area of plasma membrane was calculated from measurements of the respective lengths and expressed as a percentage.

Radioimmunoassay of l 7P-estradiol and progester­one was carried out as previously described. 13

Volume 153 Number 4

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Uterine activity and gap junctions in peripartal sheep 449

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Fig. 1. Composite of six recordings from a single ewe at different times before (AP) and after (PP) delivery. Each tracing shows, from top to bottom, the intrauterine pressure signal and the myometrial electrical activities from the fundal (A), medial (B), and cervical (C) region.

All data were time-related to parturition. The paired Student's t test was used for statistical analysis of dif­ferences between apparent conduction velocity, rate of rise, and active pressure area of intrauterine pressure cycles before, during, and after parturition. Percent­ages of gap junction area in myometrial biopsies ob­tained at different days before and after parturition were compared with those obtained during labor by means of Student's t test. Values of p < 0.05 were con­sidered significant.

Results The preparation lasted 2 to 3 weeks, but because of

malfunction of the electrodes only five ewes provided complete recordings before, during, and after partu­rition, which were used for subsequent analysis. Fig. 1 shows tracings of electrical myometrial and intrauterine

pressure signals from fundal, medial, and cervical re­gions recorded at various time intervals before, during, and after labor in a single ewe. The sequence of onset of bursts from the three regions appeared to be vari­able. The electrical myometrial bursts corresponded to changes in intrauterine pressure. More than 30 hours before delivery the electrical myometrial bursts and in­trauterine pressure cycles were infrequent (one or two cycles per hour) and oflong duration (5 to 12 minutes).

Fig. 2, A, shows the duration and Fig. 2, B, the fre­quency of the electrical myometrial bursts and intra­uterine pressure cycles before, during, and following labor at the various regions. Although some variation was observed between different ewes, there was a con­sistent decrease in duration and an increase in fre­quency of electrical myometrial bursts and intrauterine pressure cycles in all animals, starting approximately 1

450 Verhoeff et al. October 15, 1985

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day before delivery to reach minimum (duration) and

maximum (frequency) values during labor. After de­livery the frequency of electrical myometrial bursts and intrauterine pressure cycles gradually decreased; 4 days following parturition no activity could be demon­strated. There were small and inconsistent differences between the durations of the electrical myometrial bursts from the three regions obtained until 2 days before delivery. From that time, through delivery and during the first 2 days after delivery, the electrical myo­metrial variables obtained from the three regions were equal and closely related to intrauterine pressure.

The apparent conduction velocity, the active pres­sure area, and the rate of rise of the intrauterine pressure cycles are shown in Fig. 3. All three variables increased significantly I to 2 days before delivery to reach maximum values at delivery, and to decline within 3 days thereafter. The three variables show a close temporal relationship to the changes in relative gap junction area.

Plasma levels of progesterone and 1713-estradiol mea­sured before, during, and after parturition are sum­marized in Fig. 4. Progesterone levels began to fall at approximately 4 days before delivery, but the steepest

Volume 153 Number 4

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Uterine activity and gap junctions in peripartal sheep 451

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fall occurred at approximately 12 hours before deliv­ery, coinciding with a sharp rise of the estrogen levels.

Table I shows the total length of the plasma mem­brane surveyed, the total length of gap junction mem­brane, and the relative gap junction area. Gap junctions were found at all times but the relative gap junction area was significantly elevated during parturition as compared to other times before and following delivery. The increase in relative gap junction area appeared to

start 2 to 3 days before delivery and had completely disappeared I to 2 days after parturition. Figs. 3 and 4 show the close temporal relationship between gap junction area, the course of variables of uterine activity, and steroid hormone levels in the peripartum period. Fig. 5 shows a high-magnification photograph of a gap junction between myometrial cells of fundal tissue,

taken immediately post partum. No differences be­tween the volume occupied by muscle cells or between their basic structures were apparent in the various re­gions examined.

Comment The present study shows that labor in the ewe is

associated with changes in plasma levels of progester­one and estrogen, an increase in myometrial gap junc­tion area, and an increase in electrical and mechanical activity of the uterus. From the results of studies in rats and rabbits, Csapo and Takeda14 concluded that elec­trical and mechanical events of the myometrium were local, nonpropagating and asynchronous prior to labor and that the onset of labor was characterized by the gradual evolution of synchronized myometrial activity.

452 Verhoeff et al.

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Fig. 4. Means ( ± SEM) of maternal plasma levels of proges­terone (P) and 1713-estradiol (E,) before, during, and after delivery. Compare to gap junction area in Fig. 3.

In the present study in chronically instrumented preg­nant ewes we observed a good correspondence between long-lasting electrical myometrial bursts recorded from various sites of the myometrium before the animals were in labor. Similar observations in ewes have been reported by others. 15 In rabbits a similar pattern of long bursts occurring during pregnancy has been reported.8

These bursts are not necessarily propagated events. Harding et al. 15 suggest humoral control or stimulation by a nerve net, because an isolated part of a nonpreg­nant horn showed bursts occurring synchronously with those in the body of the uterus. The relatively low am­plitude of corresponding intrauterine pressure cycles observed in pregnancy until a few days before labor may be explained by uncoordinated contraction of the myometrial muscle cells.

The apparent conduction velocity measured in our experiments is similar to that reported previously for the rabbit. 14 The observation of a close relationship be­tween apparent conduction velocity and percentage gap junction area (Fig. 3) suggests that the increase in gap junction area improves the spread of electrical ac­tivity across the myometrium. However, the values ob­tained should be interpreted with care, since the pri­mary electrical event could be initiated between two electrodes and the pathway of conduction need not be

October 15, 1985 Am J Obstet Gynecol

straight. For this reason the term "apparent" conduc­tion velocity is used. We could not demonstrate a dom­inant direction of conduction, which may be due to the relatively large distance between the electrodes (20 to 30 cm). Other investigators16 reported a greater prop­agation in the tubocervical direction during labor.

The total active pressure area of the intrauterine pressure cycles (Fig. 3) during l hour is a reflection of the myometrial effort during that time. The active pres­sure area and the rate of rise of intrauterine pressure cycles measured after delivery are not comparable with the same variables obtained before delivery. The wall tension needed to build up a certain intrauterine pres­sure will be less as the uterine cavity becomes smaller and the myometrial muscle cells are shortened. This must also be taken into account in the interpretation of the values of apparent conduction velocity after de­livery.

The rate of rise of the intrauterine pressure cycles is considered to reflect recruitment of muscle cells.' There appears to be a close relationship between the rate of rise and the relative gap junction area (Fig. 3), which suggests that the formation of gap junctions im­proves the coordination of the smooth muscle cells.

The hormonal changes in plasma observed in this study are similar to those reported by others. 1•

2•

9 The present study does not prove that the changes in hor­mone levels are responsible for the increase in myo­metrial gap junction area. The temporal relationship between the changes in hormone levels and the increase in gap junction area shortly before labor must be in­terpreted with care, as only one sample was taken for measurement of gap junctions in the days immediately prior to labor. However, as in prior studies9 there is a good relationship between changes in hormone levels and the increase in gap junctions. Previous studies show that progesterone inhibits and estrogens stimulate the development of gap junctions.s. 11

• 12 Thus our results

confirm previous investigations supporting the hypoth­esis that steroid hormones regulate the formation of myometrial gap junctions.

Our study shows that the area of gap junctions in animals at delivery is approximately twice that present before and after labor (Table I). In other studies very low numbers of gap junctions were found in the an­tepartum and postpartum periods in sheep9 and other animals.4

· 5 The higher number of gap junctions prior

to labor in this study cannot be attributed to either operation or the introduction of recording devices be­cause the values were already relatively high at the time of first surgery. However, these levels were not suffi­cient to initiate or support labor. The area of gap junc­tions found during labor of approximately 0.2% (Table I) is similar to that reported for various animals,..9 and

Volume 153 Number 4

Uterine activity and gap junctions in peripartal sheep 453

Fig. 5. Electron micrograph of myometrial tissue sample taken during labor showing a gap junction with a typical seven-lined appearance. (Original magnification x 144,000.)

Table I. Number and area of gap junctions in pregnant and postpartum sheep myometrium

Total length of Total length of No. plasma gap junction Relative area

No. of of No. of gap membrane membrane of gap junction Day of sampling animals tissues junctions surveyed ( µ.m) (µ.m) membrane (%) p*

Day of gestation (first operation) 110-113 3 8 18 7,613 3,105 0.078 ± 0.027 <0.004 117 3 8 24 7,596 4,110 0.108 ± 0.019 <0.02 122-124 4 10 23 9,455 4,680 0.099 ± 0.048 <0.05

2-3 Days before 3 7 11 6,251 1,815 0.048 ± 0.019 <0.001 delivery

During labor 8 42 147 33,638 32,365 0.198 ± 0.006 Days after delivery

1-2 5 11 7 8,470 0,815 0.021 ± 0.011 <0.001 4-5 3 5 8 4,864 1,200 0.049 ± 0.017 <0.001

*p values indicate levels of significance between gap junction areas during delivery compared to those at other times.

humans, 10 indicating that there is a critical and similar number of gap junctions needed to sustain labor in different species.

The present study shows that labor in the ewe is associated with changes in plasma levels of progester­one and estrogen, with a concomitant increase in myo­metrial gap junction area as well as in electrical and mechanical activity of the uterus. These results support the hypothesis that changes in plasma and tissue levels of steroid hormones lead to an increase in muscle cell gap junction area, which improves conditions favoring coordination of contractile activity of the uterus during parturition.• It is likely that the increase in gap junction

area is one of several events necessary to increase uter­ine contractility.

We gratefully acknowledge the technical support of Miss E. Cappon, Mrs. P. Rotmans, Mr. P. C. Struyk, Mr. C. van Kooten, and Miss D. Merrett.

REFERENCES I. Liggins GC, Fairclough RJ, Grieves SA, Forster CS, Knox

BS. Parturition in sheep. In: The fetus and birth, Ciba Foundation symposium 47. Amsterdam: Elsevier, 1977: 5-30.

2. Thorburn GD, Challis JRG. Endocrine control of partu­rition. Physiol Rev l 979;59:863.

3. Csapo Al. Force of labor. In: Iffy L, Kamienetzky HA,

Verhoeff et al.

eds. Principles and practice of obstetrics and perinatology. New York: John Wiley & Sons, 1981:761-99.

4. Garfield RE, Sims SM, Daniel EE. Gap junctions: their presence and necessity in myometrium during parturi­tion. Science 1977;198:958.

5. Garfield RE, Sims SM, Kannan MS, Daniel EE. Possible role of gap junctions in activation of myometrium during parturition. Am J Physiol I 978;235:C 168.

6. Sims SM, Daniel EE, Garfield RE. Improved electrical coupling in uterine smooth muscle is associated with in­creased numbers of gap junctions at parturition. J Gen Physiol l 982;80:353.

7. Puri CP, Garfield RE. Changes in hormone levels and gap junctions in the rat uterus during pregnancy and partu­rition. Biol Reprod 1982;27:967.

8. Demianczuk N, Towell ME, Garfield RE. Myometrial elec­trophysiologic activity and gap junctions in the pregnant rabbit. AMJ 0BSTET GYNECOL 1984;149:485.

9. Garfield RE, Rabideau S, Challis JRG, Daniel EE. Hor­monal control of gap junction formation in sheep myo­metrium during parturition. Biol Reprod 1979;21:999.

IO. Garfield RE, Hayashi RH. Appearance of gap junctions in the myometrium of women during labor. AM J OBSTET GYNECOL 1981;140:254.

October 15, 1985 Am J Obstet Gynecol

I I. Garfield RE, Kannan MS, Daniel EE. Gap junction for­mation in myometrium: Control by estrogens, progester­one and prostaglandins. AmJ Physiol 1980;238:C8l.

12. Garfield RE, Puri CP, Csapo Al. Endocrine, structural, and functional changes in the uterus during premature labor. AMJ 0BSTETGYNECOL 1982;142:21.

13. De Jong FH, Baird DT, Van der Molen HJ. Ovarian se­cretion rates of estrogens, androgens and progesterone in normal women and in women with persistent ovarian follicles. Acta Endocrinol 1974;77:574.

14. Csapo Al, Takeda H. Effect of progesterone on the elec­trical activity and intrauterine pressure of pregnant and parturient rabbits. AMJ OBSTET GYNECOL 1965;91:221.

15. Harding R, Poore ER, Bailey A, Thorburn GD, Jansen CAM, Nathanielsz PW. Electromyographic activity of the non pregnant and pregnant sheep uterus. AM J OBSTET GYNECOL 1982;142:448.

16. PrudHomme MJ, Bose MJ. Motricite uterine de la Brebis, avant, pendant et apres la parturition spontanee apres traitement par la dexamethasone. Ann Biol Biochem Bio­phys 1977;17:9.

Evoked fetal startle response: A possible intrauterine

neurological examination

Michael Y. Divon, M.D., Lawrence D. Platt, M.D., Cathy J. Cantrell, M.D.,

Carl V. Smith, M.D., Sze-Ya Yeh, M.D., and Richard H. Paul, M.D.

Los Angeles, Calif omia

The fetal startle reflex was studied in an attempt to provide an objective and quantitative estimate of the

fetal neurological condition. This reflex is a normal response to a combined sound-vibratory stimulus in the

healthy infant born after 30 weeks of gestation. It consists of a generalized paroxysmal motion that

involves the whole body. Thirty women with uncomplicated pregnancies, who subsequently delivered

healthy infants, were studied at term. Fetal movements were monitored by means of a real-time scanner.

Placement of the transducer was such that it allowed for visualization of the long axis of the fetal forearm.

A 3-second stimulus was delivered on the maternal abdomen over the fetal head with use of an artificial

larynx. This device generates a mixed sound-vibratory output of 100 dB and 85 Hz. Sufficient visualization

of the plane of forearm motion was possible 68% of the time, thus allowing for measurement of the

duration of this motion. The results indicate that the mean duration of forearm motion in response to a

3-second sound-vibratory stimulus is 8.2 ± 2.3 seconds ( ± SEM). Since an immediate forearm motion was

detected each time that a stimulus was applied, we conclude that the startle reflex does indeed exist in the

fetus. This simple means of assessing the neurological state of the fetus may provide a way to evaluate

fetal tone as it applies to antenatal fetal assessment. (AM J 0BSTET GvNECOL 1985;153:454-6.)

Key words: Startle reflex, sound-vibratory stimulus, fetus, neurological condition

From the Department of Obstetrics and Gynecology, University of Southern California School of Medicine, and Women's Hospital,

Los Angeles County/University of Southern California Medical

Center. Sponsored by the Society for Gynecologic Investigation. Reprint requests: Dr. Michael Y. Divon, Room 501, Building B,

Albert Einstein College of Medicine, 1300 Morris Park Ave.,

Bronx, NY 10461.

The ability to evaluate fetal condition is of major

importance to those who provide health care to preg­

nant women. Several testing methods are presently

used in antepartum assessment of fetal well-being.

These include analysis of fetal heart rate by means of

( 1) the nonstress test, (2) the contraction stress test, and

(3) the fetal biophysical profile. 1-3 The fetal biophysical