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Electrical activity in the human oviduct after the menopause
Mururrru~, 5 (1984) 185 -191 Elsevier
185
MAT 00290
Electrical activity in the human oviduct after the menopause Antti
Talo
’ and Martti
0. Pulkkinen
2**
’ Laboratory of Animal Physiology, Department of Biology and ’ Department of Obstetrrcs and Gynaecologv, University of Turku SF- 20520 Turku, Finland (Received
2 September
1983; accepted
after revision 20 October
1983)
Electrical activity was recorded in 18 morphologically normal human oviducts excised from 17 women during hysterectomy. All women were in the first five years after menopause. The first part of the oviduct to become inactive after menopause was the isthmus near the uterus or the ampullary-isthmic junction. The region which exhibited electrical activity last was the ovarian end of the tube. The typical wave-form of electrical activity in post-menopausal oviducts resembled that recorded during the follicular phase in fertile women: a single smooth wave lasting 3-5s. In three cases, over a bulbous swelling of the ampulla, this typical activity was replaced by continuous, high frequency activity. A hypothesis is provided that the observed changes in electrical activity may be related to certain clinical phenomena such as the increased incidence of tubal pregnancy in the pre-menopause. (Key words:
Electrical
activity,
Human
oviduct,
Menopause)
Introduction The electrical activity of reflects its force [l]. In a during the menstrual cycle. activity and the form of the
the human oviduct precedes the mechanical activity, and previous study we estimated the myoelectrical activity The probability of spread towards the uterus, pacemaker electrical activity changed during the course of the cycle
111. Before and after the menopause endocrinological changes as luteal insufficiency, gradual cessation of ovulation and progesterone effect, and gradual decrease of estrogens together with an increase in the secretion of gonadotrophins may modify oviductal activity measured as electrical activity. Changes in electrical activity may provide a functional basis to certain clinical phenomena at the pre-menopause, such pregnancies [2,3]. This study as the increased relative frequency of extrauterine describes the electrical activity of the human oviduct after menopause. Material and methods A study was made of eighteen morphologically women during hysterectomy and salpingectomy * To whom correspondence 0378-5122/84/$03.00
normal oviducts, excised from 17 for various gynecological disorders
should be addressed.
0 1984 Elsevier Science Publishers
B.V.
not related to the oviduct. The age of the women varied from 49-54 yr (51.2 + 0.5, mean * SEM). The histology of the endometrium was used as a criterion for the endocrinological stage. In 12 of the patients the endometrium was of the proliferative type and in 5 it was atrophic. The time-lag from the last menstrual period varied from 1.5 mth to 5 yr. Methods of recording and the analysis of the data were the same as in the previous study [l]. After removal the oviduct was placed in oxygenated Ringer solution. The ligaments surrounding the oviduct were removed in order to expose the circular muscle layer and the recordings were made in a tissue bath containing oxygenated (95% 0, + 5% CO,) Ringer solution at 37 k 0.5”C. Six flexible suction electrodes were used simultaneously, together with a single common reference electrode in the bath. Recordings were made on a Grass 7P Polygraph. High-pass filtering (time constant of 0.45 or 2.0 s) was used, and a short direct-current recording was made in order to reveal the unfiltered wave shape. The distances between the electrodes were between 3-6 mm. The recording at each location lasted for 30-45 min. When the set of electrodes was moved, two positions remained unchanged for the next recordings. When all the recordings had been carried out the oviduct was moved into a Petri dish; both ends of the oviduct were attached to the bottom of the dish, and the tube was opened longitudinally. The length of the oviduct and the location of the ampullary-isthmic junction were determined. The location of each recording point could then be expressed on a percentage-length scale, where 0% denotes the ostium and 100% the tubo-uterine junction. Results It was possible to demonstrate electrical activity in every post-menopausal human oviduct, in most cases even along the total length of the tube. The activity consisted
Fig. 1. Different wave shapes of electrical activity in post-menopausal tubes. A and B. Recordings from the same oviduct at 40 and 90% distance from the fimbriae (100% = tubo-uterine junction). C. This shows a case where two waves combine. D and E. Recordings from the same area but higher speed in E. Small spikes can be seen in E on the top of the slow wave. All are direct current recordings; time axis = s.
187
typically of a single smooth wave lasting 3-5 s (Figs. 1. 2). Sometimes two waves became combined, forming a double peaked wave. In the ampulla of two oviducts (6 and 18 mth after last menstrual period) small atypical spikes were observed on the top of a slow wave (Fig. 1). Figure 2 shows electrical activity along one highly active oviduct. 3 mth after menopause. Electrical activity initiated under or near electrode locations 3, 10. 14 and 17 (occasionally under location l), and spread either in one or in both directions. These locations, therefore were defined as pacemakers. An analysis of the data from these recordings is given in Fig. 3. It shows the frequency of electrical activity, frequency of pacemaker activity, probability of spread toward the uterus, and velocity of spread along the oviduct. When the electrodes were placed about
0 0 0 0 0 0 0 0 0 0 0 0
Fig. 2. A composite of four original recordings covering the length of the tube. Subsequent recordings separated by continuous lines. The recording sequence from top to bottom. Pacemaker activity indicated by small circles at recording points 1, 3, 10, 14 and 17. Arrows indicate direction of spread. Duration of recording 6 min.
,0.8 + i 0.6 5 a 0.4 0 go.2
4 z G 0 iii *
3 2 1
Fig. 3. Analyses of oviductal recordings from Fig. 2. Frequency of electrical activity declining in the isthmus. Frequency of pacemaker activity shows two peaks. Note that probability of prouterine spread is high on the uterine side of the pacemakers and low on the ovarian side. Values for conduction velocity (mm/s) are means and SEM values are covered by the dots. Oviduct length in percentages (100% = tubo-uterine junction). AIJ = ampullary-isthmic junction.
equal distances apart in order to record simultaneously from all parts of the tube, isthmic activity was low. This activity increased during the subsequent recordings, starting from the ampulla near the fimbriae. The isthmic frequency during the last recording (recording points 12-17, Fig. 2) was more than l/mm. In Fig. 3, two peaks of pacemaker activity are seen in the ampulla and in the isthmus with low pacemaker activity between the peaks. The probability of spread towards the uterus is high on the uterine side of the pacemakers and low on the ovarian side. The mean velocity of spread of electrical activity, varying between 0.5 and 3.0 mm/s, was higher in the isthmus than in the ampulla. Figure 4 shows the variation of frequency of electrical activity along an oviduct 18 mth after the last menstrual period. This is a typical example of low activity in the tube.
189
50 %
loo
Fig. 4. Variation of frequency along an oviduct 18 mth after last menstrual period. A composite sequential recordings. Low frequency or absence of activity at the isthmic end of the oviduct.
of four
The isthmic activity is limited to a narrow region, the ampullary-isthmic junction is inactive and there are narrow inactive regions in the ampulla, where the frequency is highly variable. In some instances the isthmus was completely inactive, and oviductal activity occurred only in the vicinity of the fimbriae. In three oviducts, a thin-walled bulbous swelling was observed in the ampulla, near the fimbrial end. The electrical activity in these regions differed from that in the rest of the oviduct by having an almost sinewave shape and high frequency (Fig. 5). This type of activity was confined to the dilated area and it did not reach the adjacent segments. During the first 2 mth (n = 5) and after 1 yr (n = 5) after menopause, oviductal activity was characterized by high frequency near the fimbrial end, a steep decline in frequency towards the ampullary-isthmic junction and an almost total lack of activity in the isthmus (Fig. 6). Three to twelve months after the last menstrual period (n = S), there was no difference from the other groups in the mean frequency of the ampulla, but the isthmus was slightly more active. There was no correlation
Fig. 5. Electrical activity over an area where the ampulla was dilated. 54-yr-old patient. Locations of the electrodes illustrated schematically (left). Numbers on the right indicate distances between the electrodes in nm. Time scale: s.
190
4
1.5-2
months
Fig. 6. Frequency of electrical activity along the human oviduct at different times after last menstrual period. The topmost graph is the mean of the whole material. Vertical bars indicate SEM. In the groups 1.5-2 mth and 1.5-5 yr after menopause the values without SEM are due to single active oviducts.
between endometrial the oviduct.
findings
(proliferative
or atrophic)
and the electrical
activity
of
Discussion The present findings suggest that electrical (and therefore also contractile) activity persists in the human oviduct for at least a few years after menopause, but these results do not exclude a decline in contractile force during the same period. The general sequence of events in the electrical activity of the human oviduct after near the uterus or the menopause seems to be as follows: first the isthmus ampullary-isthmic junction becomes inactive; This inactive area enlarges towards the ovary, then narrow segments of the ampulla become inactive. The region which becomes inactive last is the ovarian end of the tube.
191
The wave-form of the electrical activity (single smooth wave) of postmenopausal oviducts resembles that recorded during the follicular phase in fertile women [l]. Our results confirm that the electrical activity in an estrogen-dominated human oviduct has a characteristic wave-form. The high-frequency activity over the thin-walled bulbous swellings of the ampulla is an interesting exception of otherwise consistent activity and its cause needs to be investigated. It seems possible that the ‘order’ in which the oviduct becomes inactive (isthmus first, fimbrial end last) may play a functional aetiological role in the clinical finding that the relative frequency of extrauterine pregnancies increases during the premenopause [2,3]. This can be a general model for the functional bases of extrauterine pregnancies, in cases where the tube is macroscopically and microscopically normal.
Acknowledgements We are grateful to Ms. Sinikka supported by Turun Yliopistostitio.
Hillgren for technical assistance. This study was A.T. is a Research Fellow of Suomen Akatemia.
References 1 Talo A, Pulkkinen MO. Electrical activity in the human oviduct during the menstrual cycle. Am J Obstet Gynecol 1982; 142: 135-147. 2 Timonen S, Nieminen U. Tubal pregnancy, choice of operative method of treatment. Acta Obstet Gynecol Stand 1960; 46: 327-333. 3 Niles JH, Clark JFJ. Pathogenesis of tubal pregnancy. Am J Obstet Gynecol 1969; 105: 1230-1234.
185
MAT 00290
Electrical activity in the human oviduct after the menopause Antti
Talo
’ and Martti
0. Pulkkinen
2**
’ Laboratory of Animal Physiology, Department of Biology and ’ Department of Obstetrrcs and Gynaecologv, University of Turku SF- 20520 Turku, Finland (Received
2 September
1983; accepted
after revision 20 October
1983)
Electrical activity was recorded in 18 morphologically normal human oviducts excised from 17 women during hysterectomy. All women were in the first five years after menopause. The first part of the oviduct to become inactive after menopause was the isthmus near the uterus or the ampullary-isthmic junction. The region which exhibited electrical activity last was the ovarian end of the tube. The typical wave-form of electrical activity in post-menopausal oviducts resembled that recorded during the follicular phase in fertile women: a single smooth wave lasting 3-5s. In three cases, over a bulbous swelling of the ampulla, this typical activity was replaced by continuous, high frequency activity. A hypothesis is provided that the observed changes in electrical activity may be related to certain clinical phenomena such as the increased incidence of tubal pregnancy in the pre-menopause. (Key words:
Electrical
activity,
Human
oviduct,
Menopause)
Introduction The electrical activity of reflects its force [l]. In a during the menstrual cycle. activity and the form of the
the human oviduct precedes the mechanical activity, and previous study we estimated the myoelectrical activity The probability of spread towards the uterus, pacemaker electrical activity changed during the course of the cycle
111. Before and after the menopause endocrinological changes as luteal insufficiency, gradual cessation of ovulation and progesterone effect, and gradual decrease of estrogens together with an increase in the secretion of gonadotrophins may modify oviductal activity measured as electrical activity. Changes in electrical activity may provide a functional basis to certain clinical phenomena at the pre-menopause, such pregnancies [2,3]. This study as the increased relative frequency of extrauterine describes the electrical activity of the human oviduct after menopause. Material and methods A study was made of eighteen morphologically women during hysterectomy and salpingectomy * To whom correspondence 0378-5122/84/$03.00
normal oviducts, excised from 17 for various gynecological disorders
should be addressed.
0 1984 Elsevier Science Publishers
B.V.
not related to the oviduct. The age of the women varied from 49-54 yr (51.2 + 0.5, mean * SEM). The histology of the endometrium was used as a criterion for the endocrinological stage. In 12 of the patients the endometrium was of the proliferative type and in 5 it was atrophic. The time-lag from the last menstrual period varied from 1.5 mth to 5 yr. Methods of recording and the analysis of the data were the same as in the previous study [l]. After removal the oviduct was placed in oxygenated Ringer solution. The ligaments surrounding the oviduct were removed in order to expose the circular muscle layer and the recordings were made in a tissue bath containing oxygenated (95% 0, + 5% CO,) Ringer solution at 37 k 0.5”C. Six flexible suction electrodes were used simultaneously, together with a single common reference electrode in the bath. Recordings were made on a Grass 7P Polygraph. High-pass filtering (time constant of 0.45 or 2.0 s) was used, and a short direct-current recording was made in order to reveal the unfiltered wave shape. The distances between the electrodes were between 3-6 mm. The recording at each location lasted for 30-45 min. When the set of electrodes was moved, two positions remained unchanged for the next recordings. When all the recordings had been carried out the oviduct was moved into a Petri dish; both ends of the oviduct were attached to the bottom of the dish, and the tube was opened longitudinally. The length of the oviduct and the location of the ampullary-isthmic junction were determined. The location of each recording point could then be expressed on a percentage-length scale, where 0% denotes the ostium and 100% the tubo-uterine junction. Results It was possible to demonstrate electrical activity in every post-menopausal human oviduct, in most cases even along the total length of the tube. The activity consisted
Fig. 1. Different wave shapes of electrical activity in post-menopausal tubes. A and B. Recordings from the same oviduct at 40 and 90% distance from the fimbriae (100% = tubo-uterine junction). C. This shows a case where two waves combine. D and E. Recordings from the same area but higher speed in E. Small spikes can be seen in E on the top of the slow wave. All are direct current recordings; time axis = s.
187
typically of a single smooth wave lasting 3-5 s (Figs. 1. 2). Sometimes two waves became combined, forming a double peaked wave. In the ampulla of two oviducts (6 and 18 mth after last menstrual period) small atypical spikes were observed on the top of a slow wave (Fig. 1). Figure 2 shows electrical activity along one highly active oviduct. 3 mth after menopause. Electrical activity initiated under or near electrode locations 3, 10. 14 and 17 (occasionally under location l), and spread either in one or in both directions. These locations, therefore were defined as pacemakers. An analysis of the data from these recordings is given in Fig. 3. It shows the frequency of electrical activity, frequency of pacemaker activity, probability of spread toward the uterus, and velocity of spread along the oviduct. When the electrodes were placed about
0 0 0 0 0 0 0 0 0 0 0 0
Fig. 2. A composite of four original recordings covering the length of the tube. Subsequent recordings separated by continuous lines. The recording sequence from top to bottom. Pacemaker activity indicated by small circles at recording points 1, 3, 10, 14 and 17. Arrows indicate direction of spread. Duration of recording 6 min.
,0.8 + i 0.6 5 a 0.4 0 go.2
4 z G 0 iii *
3 2 1
Fig. 3. Analyses of oviductal recordings from Fig. 2. Frequency of electrical activity declining in the isthmus. Frequency of pacemaker activity shows two peaks. Note that probability of prouterine spread is high on the uterine side of the pacemakers and low on the ovarian side. Values for conduction velocity (mm/s) are means and SEM values are covered by the dots. Oviduct length in percentages (100% = tubo-uterine junction). AIJ = ampullary-isthmic junction.
equal distances apart in order to record simultaneously from all parts of the tube, isthmic activity was low. This activity increased during the subsequent recordings, starting from the ampulla near the fimbriae. The isthmic frequency during the last recording (recording points 12-17, Fig. 2) was more than l/mm. In Fig. 3, two peaks of pacemaker activity are seen in the ampulla and in the isthmus with low pacemaker activity between the peaks. The probability of spread towards the uterus is high on the uterine side of the pacemakers and low on the ovarian side. The mean velocity of spread of electrical activity, varying between 0.5 and 3.0 mm/s, was higher in the isthmus than in the ampulla. Figure 4 shows the variation of frequency of electrical activity along an oviduct 18 mth after the last menstrual period. This is a typical example of low activity in the tube.
189
50 %
loo
Fig. 4. Variation of frequency along an oviduct 18 mth after last menstrual period. A composite sequential recordings. Low frequency or absence of activity at the isthmic end of the oviduct.
of four
The isthmic activity is limited to a narrow region, the ampullary-isthmic junction is inactive and there are narrow inactive regions in the ampulla, where the frequency is highly variable. In some instances the isthmus was completely inactive, and oviductal activity occurred only in the vicinity of the fimbriae. In three oviducts, a thin-walled bulbous swelling was observed in the ampulla, near the fimbrial end. The electrical activity in these regions differed from that in the rest of the oviduct by having an almost sinewave shape and high frequency (Fig. 5). This type of activity was confined to the dilated area and it did not reach the adjacent segments. During the first 2 mth (n = 5) and after 1 yr (n = 5) after menopause, oviductal activity was characterized by high frequency near the fimbrial end, a steep decline in frequency towards the ampullary-isthmic junction and an almost total lack of activity in the isthmus (Fig. 6). Three to twelve months after the last menstrual period (n = S), there was no difference from the other groups in the mean frequency of the ampulla, but the isthmus was slightly more active. There was no correlation
Fig. 5. Electrical activity over an area where the ampulla was dilated. 54-yr-old patient. Locations of the electrodes illustrated schematically (left). Numbers on the right indicate distances between the electrodes in nm. Time scale: s.
190
4
1.5-2
months
Fig. 6. Frequency of electrical activity along the human oviduct at different times after last menstrual period. The topmost graph is the mean of the whole material. Vertical bars indicate SEM. In the groups 1.5-2 mth and 1.5-5 yr after menopause the values without SEM are due to single active oviducts.
between endometrial the oviduct.
findings
(proliferative
or atrophic)
and the electrical
activity
of
Discussion The present findings suggest that electrical (and therefore also contractile) activity persists in the human oviduct for at least a few years after menopause, but these results do not exclude a decline in contractile force during the same period. The general sequence of events in the electrical activity of the human oviduct after near the uterus or the menopause seems to be as follows: first the isthmus ampullary-isthmic junction becomes inactive; This inactive area enlarges towards the ovary, then narrow segments of the ampulla become inactive. The region which becomes inactive last is the ovarian end of the tube.
191
The wave-form of the electrical activity (single smooth wave) of postmenopausal oviducts resembles that recorded during the follicular phase in fertile women [l]. Our results confirm that the electrical activity in an estrogen-dominated human oviduct has a characteristic wave-form. The high-frequency activity over the thin-walled bulbous swellings of the ampulla is an interesting exception of otherwise consistent activity and its cause needs to be investigated. It seems possible that the ‘order’ in which the oviduct becomes inactive (isthmus first, fimbrial end last) may play a functional aetiological role in the clinical finding that the relative frequency of extrauterine pregnancies increases during the premenopause [2,3]. This can be a general model for the functional bases of extrauterine pregnancies, in cases where the tube is macroscopically and microscopically normal.
Acknowledgements We are grateful to Ms. Sinikka supported by Turun Yliopistostitio.
Hillgren for technical assistance. This study was A.T. is a Research Fellow of Suomen Akatemia.
References 1 Talo A, Pulkkinen MO. Electrical activity in the human oviduct during the menstrual cycle. Am J Obstet Gynecol 1982; 142: 135-147. 2 Timonen S, Nieminen U. Tubal pregnancy, choice of operative method of treatment. Acta Obstet Gynecol Stand 1960; 46: 327-333. 3 Niles JH, Clark JFJ. Pathogenesis of tubal pregnancy. Am J Obstet Gynecol 1969; 105: 1230-1234.