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Am J Physiol Regul Integr Comp Physiol 294: R917-R918, 2008. First published January 23, 2008; doi:10.1152/ajpregu.00857.2007
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EDITORIAL FOCUS

DEVELOPMENTAL PHYSIOLOGY AND PREGNANCY

Is knowledge of the pattern of electrical activity in the pregnant uterus helpful to our understanding of uterine function? Focus on "Patterns of electrical propagation in the intact pregnant guinea pig uterus" by Lammers et al.

Robert E. Garfield

Reproductive Sciences Department of Obstetrics and Gynecology, University of Texas Medical Branch, Galveston, Texas

Submitted 30 November 2007 ; accepted in final form 16 January 2008

IT HAS BEEN RECOGNIZED FOR more than 60 years that electrical activity of the myometrium is the fundamental mechanism controlling uterine contractility (1). This observation has been confirmed and reaffirmed in many publications (6, 9, 12). Moreover, electrical spikes, caused by the movement of ions into and out of muscle cells, arranged into bursts, are directly responsible for contractility of the uterus during labor in pregnancy (6, 9, 12, 13). Many of these studies have expounded on the importance of electrical propagation and the contribution this makes is forceful contractions, particularly during term and preterm labor (6, 8). Marshall (12) was the first to establish that the frequency, duration, and strength of uterine contractions are directly proportional to the frequency, duration, and propagation of bursts of electrical activity. Former studies have used a variety of techniques, including micro and extracellular electrodes and other methodology where electrical activity was measured over a small area of the pregnant uterus (9, 12, 13). The recent article by Lammers, et al. (10) describes measurements of electrical activity of the term pregnant guinea pig uterus using 240 extracellular electrodes placed regularly around a large area of the whole uterus. This is an amazing feat considering acquisition, storage, and analyses of signals that occur simultaneously at 240 sites and at 1,000 samples per second for relatively long periods of time. These techniques allow them to evaluate the two-dimensional spread and patterns of propagation of signals and to calculate the velocity of conduction both in the longitudinal and circumferential directions. The studies show that propagation of individual spikes is about 7 cm/s in the longitudinal direction, where the muscle bundles lie parallel to the plane of propagation, as opposed to about 3 cm/s in the circular direction, where muscle is organized at right angles. In addition, the results demonstrate that initial electrical activity occurs more frequently along the ovarian end of the uterus and also along the antimesometrial border. The patterns of propagation are very nicely illustrated in colored images or maps that demonstrate the spatial and temporal conduction patterns of the electrical activity over large areas. Since electrical activity of the myometrium is directly responsible for contractility of the uterus, these studies clearly demonstrate how conduction controls contractility of the uterus.

It was also suggested by clinical studies accomplished by Cadeyro-Barcia et al. (3) many years ago that contractility of the uterus begins in the upper fundal region of the uterus and is conducted toward the cervix. The study conducted by Lammers et al. (10) shows that electrical activity can originate in either the ovarian or cervical end of the uterus and that propagation in either direction (i.e., toward the ovary or toward the cervix) does not affect the velocity. However, the authors indicate that initial activity occurs most often in the ovarian end (corresponding to fundus in humans). Clearly more studies on the origin and directionality of the signals are needed, and some consideration of pacemaker activity might be obtained. The present studies emphasize why propagation is so important for functionality of the contracting uterus during labor. The studies also confirm other work, using electromagnetic field analysis, which corresponds to electrical activity, done by Curtis Lowery and Hari Eswaran and colleagues on humans at the University of Arkansas (4, 5, 14). In this work, large areas of the uterus are analyzed from 151 sites noninvasively with special equipment. The patterns of electrical activity are similar to that described by Lammers et al. (10). Electrical activity of the uterus can also be recorded noninvasively by placing electrodes on the abdominal surface of pregnant patients (2, 11), but no one accomplished a study with many electrodes as done by Lammers et al. (10) in vitro. The basis for propagation and conduction of electrical signals in the uterus has been demonstrated in many structural and functional studies (6, 8) and lies in the cell-to-cell contacts (gap junctions) present between the myometrial cells. In most species, including guinea pigs, the electrical contacts between the cells are known to increase prior to labor and to form the basis for rhythmic and synchronous contractility (6, 8). In the Lammers study (10), uteri were obtained from term animals that presumably have some gap junctions, or they form in vitro during recording as suggested by the authors and shown previously (7). It would be useful to see what the patterns of propagation are like in a uterus from animals that are in the process of delivery where velocity of conduction is known to increase (13).

These studies are exceedingly useful in helping to define the migration of signals over the uterine muscle during pregnancy to control contractility. Propagation, and thereby the recruitment of muscle cells, is the key to forceful labor contractions. Future studies using this approach may include analysis of tissues from delivering animals and uteri compromised by preterm labor or conditions known to delay labor. In addition, future studies could include analysis of various treatments that either stimulate or inhibit contractility.

FOOTNOTES


Address for reprint requests and other correspondence: R. E. Garfield, Reproductive Sciences Dept. of Obstetrics and Gynecology, Univ. of Texas Medical Branch, 301 Univ. Blvd. Galveston, TX 77555-1062 (e-mail: rgarfiel{at}utmb.edu)

REFERENCES

  1. Bozler E. Electric stimulation and conduction of excitation in smooth muscle. Am J Physiol 122: 614–623, 1938.[Free Full Text]
  2. Buhimschi C, Boyle MB, Garfield RE. Electrical activity of the human uterus during pregnancy as recorded from the abdominal surface. Obstet Gynecol 90: 102–111, 1997.[CrossRef][Web of Science][Medline]
  3. Caldeyro-Barcia R, Alvarez H, Reynolds SRM. A better understanding of uterine contractility through simultaneous recording with an internal and seven channel external method. Surg Gynecol Obstet 91: 641–650, 1950.[Web of Science][Medline]
  4. Eswaran H, Preissl H, Wilson JD, Murphy P, Lowery CL. Prediction of labor in term and preterm pregnancies using non-invasive magnetomyographic recordings of uterine contractions. Am J Obstet Gynecol 190: 1598–1602, 2004.[CrossRef][Web of Science][Medline]
  5. Eswaran H, Preissl H, Wilson JD, Murphy P, Robinson SE, Lowery CL. First magnetomyographic recordings of uterine activity with spatial-temporal information with a 151-channel sensor array. Am J Obstet Gynecol 187: 145–151, 2002.[CrossRef][Web of Science][Medline]
  6. Garfield RE, Blennerhassett MG, Miller SM. Control of myometrial contractility: role and regulation of gap junctions. Oxf Rev Reprod Biol 10: 436–490, 1988.[Web of Science][Medline]
  7. Garfield RE, Merret D, Grover AK. Gap junction formation and regulation in myometrium. Am J Physiol Cell Physiol 239: C217–C228, 1980.[Abstract/Free Full Text]
  8. Garfield RE, Sims S, Daniel EE. Gap junctions: their presence and necessity in myometrium during parturition. Science 198: 958–960, 1977.[Abstract/Free Full Text]
  9. Kao CY. Electrophysiological properties of uterine smooth muscle. In: Biology of the Uterus, edited by RM Wynn and WP Jollie. New York: Plenum, 1967, 403–454.
  10. Lammers WJEP, Mirghani H, Stephen B, Dhanasekaran S, Wahab A, Sultan MA, Abazer F. Patterns of electrical propagation in the intact pregnant guinea pig uterus. Am J Physiol Regul Integr Comp Physiol. First published November 28, 2007; doi:10.1152/ajpregu.00704.2007.
  11. Maner WL, Garfield RE, Maul H, Olson G, Saade G. Predicting term and preterm delivery with transabdominal uterine electromyography. Obstet Gynecol 101: 1254–1260, 2003.[CrossRef][Medline]
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  14. Nagarajan R, Eswaran H, Wilson JD, Murphy P, Lowery CL, Preissl H. Analysis of uterine contractions: a dynamical approach. J Matern Fetal Neonatal Med 14: 8–21, 2003.[CrossRef][Medline]




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