Acta Physiol 2015, 213, 347–348
Editorial Introduction to ‘Electrical propagation in smooth muscle organs’ The present special issue of Acta Physiologica is dedicated to the introduction, approx. two decades ago, of high-resolution electrical recordings in studies on electrical propagation in smooth muscle organs, resulting in exciting new physiological and pathophysiological insights. In the years thereafter, electrical propagation studies were performed on isolated segments from the small intestine, the pregnant myometrium and the renal pelvis of the kidney (Lammers et al. 1993, 1994, 1996). Subsequently, the electrical propagation in such smooth muscle organs as rectum, stomach, ureter and the urine bladder was investigated (Lammers et al. 2006, 2009, Hammad et al. 2011, 2014). Interesting differences emerged in the pattern of propagation in each of these organs, such as in variations in pacemaker site, and in the speed, direction and extent of excitation. In the small intestines, for example, three types of electrical activation patterns could be distinguished: slow waves, and longitudinal and circular action potentials, each showing its own specific propagation pattern (Lammers et al. 2003). In more recent studies, abnormal propagation patterns were discovered in stomach and small intestines, thereby disclosing an unknown field of arrhythmias, including re-entry, in smooth muscle organs (Lammers et al. 2008, 2012). This special issue of Acta Physiologica originated from a symposium on this topic recently held at the annual meeting of the Federation of European Physiological Sciences, in Budapest, Hungary, on 28 August 2014. The symposium speakers Cheng, Lammers, Rabotti and Hammad contributed reviews on the electrical propagation in the stomach, small intestine, uterus and urological organs respectively. Schulze, Drake and Wray and their respective co-workers completed this special issue by reviewing the state of the art of such related areas as mechano-electrical coupling in the uterus, movements in the intestines and micromotions in the bladder. In the first review, Cheng (2015) describes the development of physiological research on the stomach from the visualization of contractions by Cannon and by Code, using X-rays, to Alvarez who was the first to study the electrical activation of the mammalian stomach. The origin of the slow wave is discussed, in relation to the cells responsible for this activity and their location in the stomach. Ever since, much work has been dedicated to the spread of
propagation in this organ, especially in relation to arrhythmias and their possible linkage to common diseases, such as gastroparesis. The information obtained in these studies could potentially lead to new therapies, such as electrical pacing of the diseased stomach. Lammers (2015) similarly describes the development of recording the electrical propagation in the small intestines, from Alvarez’ first in in vitro studies to the in vivo studies in animals. The pattern of normal and abnormal propagation in this very long organ is described in detail and includes the identification of different types of anatomical and functional re-entries present in this organ. Rabotti’s review (Rabotti & Massimo 2015) concentrates on the complexity of electrical propagations in the pregnant uterus, such as longitudinal vs. circumferential propagations, linear vs. circular propagations, the variable or chaotic locations of uterine pacemakers and the propagation patterns of bursts vs. individual spikes. They also describe the different types of techniques in use to record these potentials. These techniques include unipolar vs. bipolar recordings; one, two or even three dimensional recordings and finally serosal vs. cutaneous recordings. Hammad (2015) describes a series of studies performed in three urological tissues; the renal pelvis, the ureters and the bladder and reveals a surprising variety in pacemaking locations and in the spread of excitation in these three organs. It is of note that electrical propagation is not a phenomenon working in isolation. Electrical impulses originate from cells that have recently been discovered for their pacemaking function, such as the interstitial cells of Cajal (=ICC) located in the stomach and the intestines (Huizinga & Chen 2014, Sanders et al. 2014) and the ICC-like cells in other smooth muscle organs (McCloskey 2013). Furthermore, electrical impulses function to induce local contractions in smooth muscle organs. In this special issue, Schulze describes in detail the effects of contractions on the stomach and the intestine (Schulze 2015). Similarly, Vahabi and Drake review the more recent discovery of spontaneous contractions in the bladder at rest (Vahabi & Drake 2015), while Wray and colleagues describe the symphony of channels, hormones and stretches involved in the electro-mechanical coupling in the pregnant uterus to explain its quiescence during
© 2014 Scandinavian Physiological Society. Published by John Wiley & Sons Ltd, doi: 10.1111/apha.12434
347
Editorial
· W J Lammers and G J van der Vusse
pregnancy and the initiation of forceful contractions during labour (Wray et al. 2015). In summary, this special issue of Acta Physiologica provides a comprehensive overview of the current state of knowledge of the electrical propagation in smooth muscle organs. It shows several major similarities, but also interesting differences in pacemaking and propagation in these organs. Moreover, it reveals in a number of smooth muscle organs the existence of pathophysiological behaviour of electrical propagation reminiscent of cardiac arrhythmias. However, this review also shows that much more research can and should be performed to deepen our knowledge about electrical propagation in healthy and diseased smooth muscle organs. This research should also include clinical investigations and studies on other related smooth muscle organs, such as the oesophagus and the colon.
Conflict of interest There is no conflict of interests.
W. J. Lammers1 and G. J. van der Vusse2 1 Department of Physiology, College of Medicine & Health Sciences, UAE University, Al Ain, United Arab Emirates 2 Emeritus of Physiology, Cardiovascular Research Institute Maastricht, Maastricht University, Maastricht, the Netherlands E-mail: [email protected] References Cheng, L. 2015. Slow wave conduction patterns in the stomach: from Waller’s foundations to current challenges. Acta Physiol 213, 384–393. Hammad, F.T. 2015. Electrical propagation in the renal pelvis, ureter and bladder. Acta Physiol 213, 371–383. Hammad, F.T., Lammers, W.J., Stephen, B. & Lubbad, L. 2011. Propagation characteristics of the electrical impulse in the normal and obstructed ureter as determined at high electrophysiological resolution. BJU Int 108, E36–E42. Hammad, F.T., Stephen, B., Lubbad, L., Morrison, J.F. & Lammers, W.J. 2014. Macroscopic electrical propagation in the guinea pig urinary bladder. Am J Physiol Renal Physiol 307, F172–F182. Huizinga, J.D. & Chen, J.H. 2014. Interstitial cells of Cajal: an update on basic and clinical science. Curr Gastroenterol Rep 16, 363.
348
Acta Physiol 2015, 213, 347–348 Lammers, W.J. 2015. Normal and abnormal propagation in the small intestine. Acta Physiol 213, 349–359. Lammers, W.J.E.P., Al-Kais, A., Singh, S., Arafat, K. & El-Sharkawy, T.Y. 1993. Multielectrode mapping of slow wave activity in the isolated rabbit duodenum. J Appl Physiol 74, 1454–1461. Lammers, W.J.E.P., Arafat, K., El-Kays, A. & El-Sharkawy, T.Y. 1994. Spatial and temporal variations in local spike propagation in the myometrium of the 17-day pregnant rat. Am J Physiol 267, C1210–C1223. Lammers, W.J.E.P., Ahmad, H.R. & Arafat, K. 1996. Spatial and temporal variations in pacemaking and conduction in the isolated renal pelvis. Am J Physiol 270, F567–F574. Lammers, W.J.E.P., Ver Donck, L., Schuurkes, J.A.J. & Stephen, B. 2003. Longitudinal and circumferential spike patches in the canine small intestine in vivo. Am J Physiol 285, G1014–G1027. Lammers, W.J.E.P., Abazer, F., Ver Donck, L., Smets, D., Schuurkes, J.A.J. & Coulie, B. 2006. Electrical activity in the rectum of anaesthetized dogs. Neurogastroenterol Motil 18, 569–577. Lammers, W.J.E.P., Ver Donck, L., Stephen, B., Smets, D. & Schuurkes, J.A.J. 2008. Focal activities and re-entrant propagations as mechanisms of gastric tachyarrhythmias. Gastroenterology, 135, 1601–1611. Lammers, W.J.E.P., Ver Donck, L., Stephen, B., Smets, D. & Schuurkes, J.A.J. 2009. Origin and propagation of the slow wave in the canine stomach: outline of the gastric conduction system. Am J Physiol Gastrointest Liver Physiol 296, G1200–G1210. Lammers, W.J., Stephen, B.S. & Karam, S.M. 2012. Functional reentry and circus movement arrhythmia in the small intestine of the normal and diabetic rat. Am J Physiol 302, G684–G689. McCloskey, K.D. 2013. Bladder interstitial cells: an updated review of current knowledge. Acta Physiol (Oxf) 207, 7–15. Rabotti, C. & Massimo, M. 2015. Propagation of electrical activity in uterine muscle during pregnancy: a review. Acta Physiol 213, 406–416. Sanders, K.M., Ward, S.M. & Koh, S.D. 2014. Interstitial cells: regulators of smooth muscle function. Physiol Rev 94, 859–907. Schulze, K.S. 2015. Imaging patterns of gastro-intestinal movements and the computing of digestive processes. Acta Physiol 213, 394–405. Vahabi, B. & Drake, M.J. 2015. Physiological and pathophysiological implications of micromotion activity in urinary bladder function. Acta Physiol 213, 360–370. Wray, S., Burdyga, T., Noble, D., Noble, K., Borysova, L. & Arrowsmith, A. 2015. Progress in understanding electromechanical signaling in the myometrium. Acta Physiol 213, 417–431.
© 2014 Scandinavian Physiological Society. Published by John Wiley & Sons Ltd, doi: 10.1111/apha.12434
Editorial Introduction to ‘Electrical propagation in smooth muscle organs’ The present special issue of Acta Physiologica is dedicated to the introduction, approx. two decades ago, of high-resolution electrical recordings in studies on electrical propagation in smooth muscle organs, resulting in exciting new physiological and pathophysiological insights. In the years thereafter, electrical propagation studies were performed on isolated segments from the small intestine, the pregnant myometrium and the renal pelvis of the kidney (Lammers et al. 1993, 1994, 1996). Subsequently, the electrical propagation in such smooth muscle organs as rectum, stomach, ureter and the urine bladder was investigated (Lammers et al. 2006, 2009, Hammad et al. 2011, 2014). Interesting differences emerged in the pattern of propagation in each of these organs, such as in variations in pacemaker site, and in the speed, direction and extent of excitation. In the small intestines, for example, three types of electrical activation patterns could be distinguished: slow waves, and longitudinal and circular action potentials, each showing its own specific propagation pattern (Lammers et al. 2003). In more recent studies, abnormal propagation patterns were discovered in stomach and small intestines, thereby disclosing an unknown field of arrhythmias, including re-entry, in smooth muscle organs (Lammers et al. 2008, 2012). This special issue of Acta Physiologica originated from a symposium on this topic recently held at the annual meeting of the Federation of European Physiological Sciences, in Budapest, Hungary, on 28 August 2014. The symposium speakers Cheng, Lammers, Rabotti and Hammad contributed reviews on the electrical propagation in the stomach, small intestine, uterus and urological organs respectively. Schulze, Drake and Wray and their respective co-workers completed this special issue by reviewing the state of the art of such related areas as mechano-electrical coupling in the uterus, movements in the intestines and micromotions in the bladder. In the first review, Cheng (2015) describes the development of physiological research on the stomach from the visualization of contractions by Cannon and by Code, using X-rays, to Alvarez who was the first to study the electrical activation of the mammalian stomach. The origin of the slow wave is discussed, in relation to the cells responsible for this activity and their location in the stomach. Ever since, much work has been dedicated to the spread of
propagation in this organ, especially in relation to arrhythmias and their possible linkage to common diseases, such as gastroparesis. The information obtained in these studies could potentially lead to new therapies, such as electrical pacing of the diseased stomach. Lammers (2015) similarly describes the development of recording the electrical propagation in the small intestines, from Alvarez’ first in in vitro studies to the in vivo studies in animals. The pattern of normal and abnormal propagation in this very long organ is described in detail and includes the identification of different types of anatomical and functional re-entries present in this organ. Rabotti’s review (Rabotti & Massimo 2015) concentrates on the complexity of electrical propagations in the pregnant uterus, such as longitudinal vs. circumferential propagations, linear vs. circular propagations, the variable or chaotic locations of uterine pacemakers and the propagation patterns of bursts vs. individual spikes. They also describe the different types of techniques in use to record these potentials. These techniques include unipolar vs. bipolar recordings; one, two or even three dimensional recordings and finally serosal vs. cutaneous recordings. Hammad (2015) describes a series of studies performed in three urological tissues; the renal pelvis, the ureters and the bladder and reveals a surprising variety in pacemaking locations and in the spread of excitation in these three organs. It is of note that electrical propagation is not a phenomenon working in isolation. Electrical impulses originate from cells that have recently been discovered for their pacemaking function, such as the interstitial cells of Cajal (=ICC) located in the stomach and the intestines (Huizinga & Chen 2014, Sanders et al. 2014) and the ICC-like cells in other smooth muscle organs (McCloskey 2013). Furthermore, electrical impulses function to induce local contractions in smooth muscle organs. In this special issue, Schulze describes in detail the effects of contractions on the stomach and the intestine (Schulze 2015). Similarly, Vahabi and Drake review the more recent discovery of spontaneous contractions in the bladder at rest (Vahabi & Drake 2015), while Wray and colleagues describe the symphony of channels, hormones and stretches involved in the electro-mechanical coupling in the pregnant uterus to explain its quiescence during
© 2014 Scandinavian Physiological Society. Published by John Wiley & Sons Ltd, doi: 10.1111/apha.12434
347
Editorial
· W J Lammers and G J van der Vusse
pregnancy and the initiation of forceful contractions during labour (Wray et al. 2015). In summary, this special issue of Acta Physiologica provides a comprehensive overview of the current state of knowledge of the electrical propagation in smooth muscle organs. It shows several major similarities, but also interesting differences in pacemaking and propagation in these organs. Moreover, it reveals in a number of smooth muscle organs the existence of pathophysiological behaviour of electrical propagation reminiscent of cardiac arrhythmias. However, this review also shows that much more research can and should be performed to deepen our knowledge about electrical propagation in healthy and diseased smooth muscle organs. This research should also include clinical investigations and studies on other related smooth muscle organs, such as the oesophagus and the colon.
Conflict of interest There is no conflict of interests.
W. J. Lammers1 and G. J. van der Vusse2 1 Department of Physiology, College of Medicine & Health Sciences, UAE University, Al Ain, United Arab Emirates 2 Emeritus of Physiology, Cardiovascular Research Institute Maastricht, Maastricht University, Maastricht, the Netherlands E-mail: [email protected] References Cheng, L. 2015. Slow wave conduction patterns in the stomach: from Waller’s foundations to current challenges. Acta Physiol 213, 384–393. Hammad, F.T. 2015. Electrical propagation in the renal pelvis, ureter and bladder. Acta Physiol 213, 371–383. Hammad, F.T., Lammers, W.J., Stephen, B. & Lubbad, L. 2011. Propagation characteristics of the electrical impulse in the normal and obstructed ureter as determined at high electrophysiological resolution. BJU Int 108, E36–E42. Hammad, F.T., Stephen, B., Lubbad, L., Morrison, J.F. & Lammers, W.J. 2014. Macroscopic electrical propagation in the guinea pig urinary bladder. Am J Physiol Renal Physiol 307, F172–F182. Huizinga, J.D. & Chen, J.H. 2014. Interstitial cells of Cajal: an update on basic and clinical science. Curr Gastroenterol Rep 16, 363.
348
Acta Physiol 2015, 213, 347–348 Lammers, W.J. 2015. Normal and abnormal propagation in the small intestine. Acta Physiol 213, 349–359. Lammers, W.J.E.P., Al-Kais, A., Singh, S., Arafat, K. & El-Sharkawy, T.Y. 1993. Multielectrode mapping of slow wave activity in the isolated rabbit duodenum. J Appl Physiol 74, 1454–1461. Lammers, W.J.E.P., Arafat, K., El-Kays, A. & El-Sharkawy, T.Y. 1994. Spatial and temporal variations in local spike propagation in the myometrium of the 17-day pregnant rat. Am J Physiol 267, C1210–C1223. Lammers, W.J.E.P., Ahmad, H.R. & Arafat, K. 1996. Spatial and temporal variations in pacemaking and conduction in the isolated renal pelvis. Am J Physiol 270, F567–F574. Lammers, W.J.E.P., Ver Donck, L., Schuurkes, J.A.J. & Stephen, B. 2003. Longitudinal and circumferential spike patches in the canine small intestine in vivo. Am J Physiol 285, G1014–G1027. Lammers, W.J.E.P., Abazer, F., Ver Donck, L., Smets, D., Schuurkes, J.A.J. & Coulie, B. 2006. Electrical activity in the rectum of anaesthetized dogs. Neurogastroenterol Motil 18, 569–577. Lammers, W.J.E.P., Ver Donck, L., Stephen, B., Smets, D. & Schuurkes, J.A.J. 2008. Focal activities and re-entrant propagations as mechanisms of gastric tachyarrhythmias. Gastroenterology, 135, 1601–1611. Lammers, W.J.E.P., Ver Donck, L., Stephen, B., Smets, D. & Schuurkes, J.A.J. 2009. Origin and propagation of the slow wave in the canine stomach: outline of the gastric conduction system. Am J Physiol Gastrointest Liver Physiol 296, G1200–G1210. Lammers, W.J., Stephen, B.S. & Karam, S.M. 2012. Functional reentry and circus movement arrhythmia in the small intestine of the normal and diabetic rat. Am J Physiol 302, G684–G689. McCloskey, K.D. 2013. Bladder interstitial cells: an updated review of current knowledge. Acta Physiol (Oxf) 207, 7–15. Rabotti, C. & Massimo, M. 2015. Propagation of electrical activity in uterine muscle during pregnancy: a review. Acta Physiol 213, 406–416. Sanders, K.M., Ward, S.M. & Koh, S.D. 2014. Interstitial cells: regulators of smooth muscle function. Physiol Rev 94, 859–907. Schulze, K.S. 2015. Imaging patterns of gastro-intestinal movements and the computing of digestive processes. Acta Physiol 213, 394–405. Vahabi, B. & Drake, M.J. 2015. Physiological and pathophysiological implications of micromotion activity in urinary bladder function. Acta Physiol 213, 360–370. Wray, S., Burdyga, T., Noble, D., Noble, K., Borysova, L. & Arrowsmith, A. 2015. Progress in understanding electromechanical signaling in the myometrium. Acta Physiol 213, 417–431.
© 2014 Scandinavian Physiological Society. Published by John Wiley & Sons Ltd, doi: 10.1111/apha.12434
