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A novel laparoscopic device for measuring gastrointestinal slow-wave activity
Abstract and Figures
A periodic electrical activity, termed "slow waves", coordinates gastrointestinal contractions. Slow-wave dysrhythmias are thought to contribute to dysmotility syndromes such as postoperative gastroparesis, but the clinical significance of these dysrhythmias remains poorly defined. Electrogastrography (EGG) has been unable to characterize dsyrhythmic activity reliably, and the most accurate method for evaluating slow waves is to record directly from the surface of the target organ. This study presents a novel laparoscopic device for recording serosal slow-wave activity, together with its validation.
The novel device consists of a shaft (diameter, 4 mm; length, 300 mm) and a flexible connecting cable. It contains four individual electrodes and is fully shielded. Validation was performed by comparing slow-wave recordings from the laparoscopic device with those from a standard electrode platform in an open-abdomen porcine model. An intraoperative human trial of the device also was performed by recording activity from the gastric antrum of a patient undergoing a laparoscopic cholecystectomy.
Slow-wave amplitudes were similar between the laparoscopic device and the standard recording platform (mean 0.38 ± 0.03 mV vs range 0.36-0.38 ± 0.03 mV) (p = 0.94). The signal-to-noise ratio (SNR) also was similar between the two types of electrodes (13.7 dB vs 12.6 dB). High-quality antral slow-wave recordings were achieved in the intraoperative human trial (amplitude, 0.41 ± 0.04 mV; SNR, 12.6 dB), and an activation map was constructed showing normal aboral slow-wave propagation at a velocity of 6.3 ± 0.9 mm/s.
The novel laparoscopic device achieves high-quality serosal slow-wave recordings. It is easily deployable and atraumatic. It is anticipated that this device will aid in the clinical investigation of normal and dsyrhythmic slow-wave activity. In particular, it offers new potential for investigating the effect of surgical procedures on slow-wave activity.
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... The adoption of minimally invasive surgical procedures for the treatment of GI diseases continues to expand. Consequently, it is essential to develop new laparoscopic devices for minimally invasive recording of slow wave activity directly from the serosal surface of the GI tract, facilitating future targeted treatment for dysrhythmias [15]. However, current laparoscopic approaches record from a limited number of electrodes covering a small spatial area (approximately 4 9 4 mm 2 ) [15,16]. ...
... Consequently, it is essential to develop new laparoscopic devices for minimally invasive recording of slow wave activity directly from the serosal surface of the GI tract, facilitating future targeted treatment for dysrhythmias [15]. However, current laparoscopic approaches record from a limited number of electrodes covering a small spatial area (approximately 4 9 4 mm 2 ) [15,16]. It is necessary to record from a larger field of electrodes to accurately define dysrhythmias and to avoid large errors when estimating the velocity of slow waves [7]. ...
... The device was manually held in position, and steadied against the laparoscopic port. The recording apparatus was set up as previously described, with reference electrodes placed on the shoulders [2,15]. Signal acquisition and quality were assessed by quantifying amplitude, velocity and frequency of slow wave events and the signal-to-noise ratio (SNR), in comparison with previous benchmarks [15,27]. ...
Background:
Gastric slow waves regulate peristalsis, and gastric dysrhythmias have been implicated in functional motility disorders. To accurately define slow wave patterns, it is currently necessary to collect high-resolution serosal recordings during open surgery. We therefore developed a novel gastric slow wave mapping device for use during laparoscopic procedures.
Methods:
The device consists of a retractable catheter constructed of a flexible nitinol core coated with Pebax. Once deployed through a 5-mm laparoscopic port, the spiral head is revealed with 32 electrodes at 5 mm intervals. Recordings were validated against a reference electrode array in pigs and tested in a human patient.
Results:
Recordings from the device and a reference array in pigs were identical in frequency (2.6 cycles per minute; p = 0.91), and activation patterns and velocities were consistent (8.9 ± 0.2 vs 8.7 ± 0.1 mm s(-1); p = 0.2). Device and reference amplitudes were comparable (1.3 ± 0.1 vs 1.4 ± 0.1 mV; p = 0.4), though the device signal-to-noise ratio was higher (17.5 ± 0.6 vs 12.8 ± 0.6 dB; P < 0.0001). In the human patient, corpus slow waves were recorded and mapped (frequency 2.7 ± 0.03 cycles per minute, amplitude 0.8 ± 0.4 mV, velocity 2.3 ± 0.9 mm s(-1)).
Conclusion:
In conclusion, the novel laparoscopic device achieves high-quality serosal slow wave recordings. It can be used for laparoscopic diagnostic studies to document slow wave patterns in patients with gastric motility disorders.
... Multisite electromyography has distinguished the 'ripples' generated by myogenic slow waves, from neurally mediated peristaltic contractions [109]. A group in New Zealand has further developed multi-electrode plates, with highly flexible sheets that can be placed directly upon an organ [138]. With this technique the group recorded slow wave activity directly from the stomach of anaesthetised human patients during surgical procedures [138]. ...
... A group in New Zealand has further developed multi-electrode plates, with highly flexible sheets that can be placed directly upon an organ [138]. With this technique the group recorded slow wave activity directly from the stomach of anaesthetised human patients during surgical procedures [138]. ...
Over 150 years ago, methods for quantitative analysis of gastrointestinal motor patterns first appeared. Graphic representations of physiological variables were recorded with the kymograph after the mid-1800s. Changes in force or length of intestinal muscles could be quantified, however most recordings were limited to a single point along the digestive tract. In parallel, photography and cinematography with X-Rays visualised changes in intestinal shape, but were hard to quantify. More recently, the ability to record physiological events at many sites along the gut in combination with computer processing allowed construction of spatiotemporal maps. These included diameter maps (DMaps), constructed from video recordings of intestinal movements and pressure maps (PMaps), constructed using data from high-resolution manometry catheters. Combining different kinds of spatiotemporal maps revealed additional details about gut wall status, including compliance, which relates forces to changes in length. Plotting compliance values along the intestine enabled combined DPMaps to be constructed, which can distinguish active contractions and relaxations from passive changes. From combinations of spatiotemporal maps, it is possible to deduce the role of enteric circuits and pacemaker cells in the generation of complex motor patterns. Development and application of spatiotemporal methods to normal and abnormal motor patterns in animals and humans is ongoing, with further technical improvements arising from their combination with impedance manometry, magnetic resonance imaging, electrophysiology, and ultrasonography.
... 29,33 Four studies of HR mapping in controls have been performed to date, all of which demonstrated normal propagation in the high majority of cases. 36,50,77,78 An important caveat is that all such HR studies (including both patient and control data) have been gathered in the fasted state, intraoperatively, and under general anesthesia. ...
... clinical translation. To this end, progressive attempts have been made to reduce invasiveness, initially by insertion of electrode arrays through a trocar during laparoscopic surgery, demonstrated as a feasible approach using porcine models and human controls 77,78 ( Figure 3B,D,E). The only study comparing patients with controls using this less-invasive laparoscopic approach was immediately before and after sleeve gastrectomy in eight subjects, 50 Figure 3F). ...
Background
Gastric motility disorders, which include both functional and organic etiologies, are highly prevalent. However, there remains a critical lack of objective biomarkers to guide efficient diagnostics and personalized therapies. Bioelectrical activity plays a fundamental role in coordinating gastric function and has been investigated as a contributing mechanism to gastric dysmotility and sensory dysfunction for a century. However, conventional electrogastrography (EGG) has not achieved common clinical adoption due to its perceived limited diagnostic capability and inability to impact clinical care. The last decade has seen the emergence of novel high‐resolution methods for invasively mapping human gastric electrical activity in health and disease, providing important new insights into gastric physiology. The limitations of EGG have also now become clearer, including the finding that slow‐wave frequency alone is not a reliable discriminator of gastric dysrhythmia, shifting focus instead toward altered spatial patterns. Recently, advances in bioinstrumentation, signal processing, and computational modeling have aligned to allow non‐invasive body surface mapping of the stomach to detect spatiotemporal gastric dysrhythmias. The clinical relevance of this emerging strategy to improve diagnostics now awaits determination.
Purpose
This review evaluates these recent advances in clinical gastric electrophysiology, together with promising emerging data suggesting that novel gastric electrical signatures recorded at the body surface (termed “body surface mapping”) may correlate with symptoms. Further technological progress and validation data are now awaited to determine whether these advances will deliver on the promise of clinical gastric electrophysiology diagnostics.
... C) Custom rigid array for in-vitro recordings, with protruding electrodes to allow free perfusion of mapped target tissue in a tissue bath [8] . Custom laparoscopic probe (D) and spiral (E) electrode arrays designed for less-invasive intra-operative deployment [66], [87]. F) A prototype spherical electrode array designed for minimally-invasive endoscopic deployment to the gastric mucosa [97]. ...
... recordings with progressively increasing areas of serosal mapping have been described. The simplest of these was a rigid probe device, employing silver wire electrodes embedded in epoxy-resin and with a shielded shaft (Fig. 3C) [87]. While this device achieved high-quality signals, the limited (subcentimeter) serosal coverage meant that only small regions could be assessed in series. ...
Over the last two decades, high-resolution (HR) mapping has emerged as a powerful technique to study normal and abnormal bioelectrical events in the gastrointestinal (GI) tract. This technique, adapted from cardiology, involves the use of dense arrays of electrodes to track bioelectrical sequences in fine spatiotemporal detail. HR mapping has now been applied in many significant GI experimental studies informing and clarifying both normal physiology and arrhythmic behaviors in disease states. This review provides a comprehensive and critical analysis of current methodologies for HR electrical mapping in the GI tract, including extracellular measurement principles, electrode design and mapping devices, signal processing and visualization techniques, and translational research strategies. The scope of the review encompasses the broad application of GI HR methods from in-vitro tissue studies to in-vivo experimental studies, including in humans. Controversies and future directions for GI mapping methodologies are addressed, including emerging opportunities to better inform diagnostics and care in patients with functional gut disorders of diverse etiologies.
... Familoni et al. presented the first laparoscopic extracellular SW recordings from the stomach and small bowel using pairs of stainless-steel electrodes [69]. In the last decade, several approaches were investigated to exploit multielectrode arrays in laparoscopic SW mapping [70,71]. Endoscopic approaches were also investigated as a minimally invasive strategy to measure SWs from the mucosal surface of the stomach [72,73]. ...
Coordinated contractions and motility patterns unique to each gastrointestinal organ facilitate the digestive process. These motor activities are coordinated by bioelectrical events, sensory and motor nerves, and hormones. The motility problems in the gastrointestinal tract known as functional gastrointestinal disorders (FGIDs) are generally caused by impaired neuromuscular activity and are highly prevalent. Their diagnosis is challenging as symptoms are often vague and difficult to localize. Therefore, the underlying pathophysiological factors remain unknown. However, there is an increasing level of research and clinical evidence suggesting a link between FGIDs and altered bioelectrical activity. In addition, electroceuticals (bioelectrical therapies to treat diseases) have recently gained significant interest. This paper gives an overview of bioelectrical signatures of gastrointestinal organs with normal and/or impaired motility patterns and bioelectrical therapies that have been developed for treating FGIDs. The existing research evidence suggests that bioelectrical activities could potentially help to identify the diverse etiologies of FGIDs and overcome the drawbacks of the current clinically adapted methods. Moreover, electroceuticals could potentially be effective in the treatment of FGIDs and replace the limited existing conventional therapies which often attempt to treat the symptoms rather than the underlying condition.
The physiological function of the gastrointestinal (GI) tract is based on the slow wave generated and transmitted by the interstitial cells of Cajal. Extracellular myoelectric recording techniques are often used to record the characteristics and propagation of slow wave and analyze the models of slow wave transmission under physiological and pathological conditions to further explore the mechanism of GI dysfunction. This article reviews the application and research progress of electromyography, bioelectromagnetic technology, and high-resolution mapping in animal and clinical experiments, summarizes the clinical application of GI electrical stimulation therapy, and reviews the electrophysiological research in the biliary system.
The gastrointestinal (GI) tract is a complex environment comprised of the mouth, esophagus, stomach, small and large intestines, rectum and anus, which all cooperate to form the complete working GI system. Access to the GI using endoscopy has been augmented over the past several decades by swallowable diagnostic electromechanical devices, such as pill cameras. Research continues today and into the foreseeable future on new and more capable miniature devices for the purposes of systemic drug delivery, therapy, tissue biopsy, microbiome sampling, and a host of other novel ground-breaking applications. The purpose of this review is to provide engineers in this field a comprehensive reference manual of the GI environment and its complex physical, biological, and chemical characteristics so they can more quickly understand the constraints and challenges associated with developing devices for the GI space. To accomplish this, the work reviews and summarizes a broad spectrum of literature covering the main anatomical and physiological properties of the GI tract that are pertinent to successful development and operation of an electromechanical device. Each organ in the GI is discussed in this context, including the main mechanisms of digestion, chemical and mechanical processes that could impact devices, and GI motor behavior and resultant forces that may be experienced by objects as they move through the environment of the gut.
Mathematical and computational modeling of the stomach is an emerging field of biomechanics where several complex phenomena, such as gastric electrophysiology, fluid mechanics of the digesta, and solid mechanics of the gastric wall, need to be addressed. Developing a comprehensive multiphysics model of the stomach that allows studying the interactions between these phenomena remains one of the greatest challenges in biomechanics. A coupled multiphysics model of the human stomach would enable detailed in‐silico studies of the digestion of food in the stomach in health and disease. Moreover, it has the potential to open up unprecedented opportunities in numerous fields such as computer‐aided medicine and food design. This review article summarizes our current understanding of the mechanics of the human stomach and delineates the challenges in mathematical and computational modeling which remain to be addressed in this emerging area.
The motility of the intestines is partly governed by a bioelectrical activity termed intestinal slow wave activity; however, the dynamics of the electromechanical relationship have remained poorly defined. With the recent advances in continuum-based multi-scale modeling techniques, we present a modeling framework to investigate the electromechanical coupling in a segment of small intestine. The overall modeling framework included three parts: (i) an anatomical model describing the geometry and makeup of the smooth muscle fibers; (ii) an electrical model describing the slow wave propagation; and (iii) a mechanical model describing the active and passive tension laws during contraction. The resultant intraluminal pressure was approximated using Lamé’s thick-walled cylinder equation. This modeling framework demonstrates the potential to be used in investigating the effects of intestinal slow wave dysrhythmias on the motility of the small intestine, and may be extended in the future to incorporate additional regulatory factors and pathways.
High-resolution, multi-electrode mapping is providing valuable new insights into the origin, propagation, and abnormalities of gastrointestinal (GI) slow wave activity. Construction of high-resolution mapping arrays has previously been a costly and time-consuming endeavor, and existing arrays are not well suited for human research as they cannot be reliably and repeatedly sterilized. The design and fabrication of a new flexible printed circuit board (PCB) multi-electrode array that is suitable for GI mapping is presented, together with its in vivo validation in a porcine model. A modified methodology for characterizing slow waves and forming spatiotemporal activation maps showing slow waves propagation is also demonstrated. The validation study found that flexible PCB electrode arrays are able to reliably record gastric slow wave activity with signal quality near that achieved by traditional epoxy resin-embedded silver electrode arrays. Flexible PCB electrode arrays provide a clinically viable alternative to previously published devices for the high-resolution mapping of GI slow wave activity. PCBs may be mass-produced at low cost, and are easily sterilized and potentially disposable, making them ideally suited to intra-operative human use.
Peristaltic motor activity of the gut is an essential activity to sustain life. In each gut organ, a multitude of overlapping mechanisms has developed to acquire the ability of coordinated contractile activity under a variety of circumstances and in response to a variety of stimuli. The presence of several simultaneously operating control systems is a challenge for investigators who focus on the role of one particular control activity since it is often not possible to decipher which control systems are operating or dominant in a particular situation. A crucial advantage of multiple control systems is that gut motility control can withstand injury to one or more of its components. Our efforts to increase understanding of control mechanism are not helped by recent attempts to eliminate proven control systems such as interstitial cells of Cajal (ICC) as pacemaker cells, or intrinsic sensory neurons, nor does it help to view peristalsis as a simple reflex. This review focuses on the role of ICC as slow-wave pacemaker cells and places ICC into the context of other control mechanisms, including control systems intrinsic to smooth muscle cells. It also addresses some areas of controversy related to the origin and propagation of pacemaker activity. The urge to simplify may have its roots in the wish to see the gut as a consequence of a single perfect design experiment whereas in reality the control mechanisms of the gut are the messy result of adaptive changes over millions of years that have created complementary and overlapping control systems. All these systems together reliably perform the task of moving and mixing gut content to provide us with essential nutrients.
Gastric electrical activity was recorded from twenty-six patients at celiotomy. The human gastric pacemaker was localized to an area in the midcorpus along the greater curve. Pacesetter potentials were generated regularly by the pacemaker at a mean frequency of 3.2 cycles/min and were propagated circumferentially and aborally from the pacemaker, increasing in amplitude and velocity as they approached the pylorus. The pattern of pacesetter potentials in patients with gastric ulcer, gastric cancer, and duodenal ulcer was similar to that of patients without such diseases. Complete transection of the gastric corpus isolated the distal stomach from the natural pacemaker and resulted in the appearance of a new pacemaker in the distal stomach with a slower frequency. The fact that proximal gastric vagotomy did not greatly alter the frequency of generation or the pattern of propagation of the pacesetter potential provided further evidence that both are myogenic phenomena.
High resolution electrical mapping in the gastrointestinal system entails recording from a large number of extracellular electrodes simultaneously. It allows the collection of signals from 240 individual sites which are then amplified, filtered, digitized, multiplexed and stored on tape. After recording, periods of interest can be analysed and the original sequence of activity reconstructed. This technology, originally developed to study normal rhythms and abnormal dysrhythmias in the heart, has been modified to allow recordings from the gastrointestinal tract. In this report, initial results are presented describing the origin and propagation of the slow wave in the isolated stomach and the isolated duodenum in the cat. These results show that in both organs it not uncommon to have more than one focus active during a single cycle. The conduction of slow waves from such a multiple pacemaker environment can become quite complex, and this may play a role in determining the contractile pattern in these organs.
The functions of the gastrointestinal (GI) tract include digestion, absorption, excretion, and protection. In this review, we focus on the electrical activity of the stomach and small intestine, which underlies the motility of these organs, and where the most detailed systems descriptions and computational models have been based to date. Much of this discussion is also applicable to the rest of the GI tract. This review covers four major spatial scales: cell, tissue, organ, and torso, and discusses the methods of investigation and the challenges associated with each. We begin by describing the origin of the electrical activity in the interstitial cells of Cajal, and its spread to smooth muscle cells. The spread of electrical activity through the stomach and small intestine is then described, followed by the resultant electrical and magnetic activity that may be recorded on the body surface. A number of common and highly symptomatic GI conditions involve abnormal electrical and/or motor activity, which are often termed functional disorders. In the last section of this review we address approaches being used to characterize and diagnose abnormalities in the electrical activity and how these might be applied in the clinical setting. The understanding of electrophysiology and motility of the GI system remains a challenging field, and the review discusses how biophysically based mathematical models can help to bridge gaps in our current knowledge, through integration of otherwise separate concepts. Copyright © 2009 John Wiley & Sons, Inc.
This article is categorized under: Physiology > Mammalian Physiology in Health and Disease
Development of gastric electrical stimulation techniques for treatment of gastric dysmotility syndromes and obesity has been a long-standing goal of investigators and clinicians. Depending on stimulus parameters and sites of stimulation, such methods have a range of theoretical benefits including entrainment of intrinsic gastric electrical activity, eliciting propagating contractions and reducing symptomatology in patients with gastroparesis and reducing appetite and food intake in individuals with morbid obesity. Additionally, gastric stimulation parameters have extragastrointestinal effects including alteration of systemic hormonal and autonomic neural activity and modulation of afferent nerve pathways projecting to the central nervous system that may represent important mechanisms of action. Numerous case series and smaller numbers of controlled trials suggest clinical benefits in these two conditions, however better controlled trials are mandated to confirm their efficacy. Current research is focusing on novel stimulation methods to better control symptoms in gastroparesis and promote weight reduction in morbid obesity.
Gastric arrhythmias occur in humans and experimental animals either spontaneously or induced by drugs or diseases. However, there is no information regarding the origin or the propagation patterns of the slow waves that underlie such arrhythmias.
To elucidate this, simultaneous recordings were made on the antrum and the distal corpus during tachygastrias in open abdominal anesthetized dogs using a 240 extracellular electrode assembly. After the recordings, the signals were analyzed, and the origin and path of slow wave propagations were reconstructed.
Several types of arrhythmias could be distinguished, including (1) premature slow waves (25% of the arrhythmias), (2) single aberrant slow waves (4%), (3) bursts (18%), (4) regular tachygastria (11%), and (5) irregular tachygastria (10%). During regular tachygastria, rapid, regular slow waves emerged from the distal antrum or the greater curvature, whereas, during irregular tachygastria, numerous variations occurred in the direction of propagation, conduction blocks, focal activity, and re-entry. In 12 cases, the arrhythmia was initiated in the recorded area. In each case, after a normal propagating slow wave, a local premature slow wave occurred in the antrum. These premature slow waves propagated in various directions, often describing a single or a double loop that re-entered several times, thereby initiating additional slow waves.
Gastric arrhythmias resemble those in the heart and share many common features such as focal origin, re-entry, circular propagation, conduction blocks, and fibrillation-like behavior.
A 5-month-old white male developed gastric retention unrelieved by either pyloromyotomy or by gastrojejunostomy. The pattern of electrical activity in the wall of the stomach recorded at a third operation was consistent with an ectopic distal antral pacemaker generating electrical cycles (pacesetter potentials, action potentials, or control potentials) at a rapid frequency of 4.7 cycles per min (tachygastria). The gastric pressure increased from 1 cm H2O to only 5 cm H2O as the stomach was distended to 600 ml, with no further increase after 0.6 mg of urecholine given subcutaneously. Resection of the distal three-fourths of the stomach and gastrojejunostomy when the patient was 1 year old allowed him to resume oral intake without vomiting and with progressive weight gain. The circular smooth muscle cells of the corpus and antrum, when tested in vitro using intracellular electrodes, generated electrical cycles at rapid frequencies of 5 and 20 cycles per min, respectively. The plateau component of the spontaneous electrical cycles which regulates contractile activity, was small or absent in both corporal and antral cells, and the size of the plateau was not increased by pentagastrin or acetylcholine given at doses suprathreshold for healthy gastric smooth muscle. Our conclusion is that the decreased plateau size of the spontaneous electrical cycles generated by the gastric smooth muscle cells and the diminished sensitivity of the cells to appropriate contractile stimuli caused this patient's gastric retention.
Gastric electrical activity was recorded from twenty-six patients at celiotomy. The human gastric pacemaker was localized to an area in the midcorpus along the greater curve. Pacesetter potentials were generated regularly by the pacemaker at a mean frequency of 3.2 cycles/min and were propagated circumferentially and aborally from the pacemaker, increasing in amplitude and velocity as they approach the pylorus. The pattern of pacesetter potenitals in patients with gastric ulcer, gastric cancer, and duodenal ulcer was similar to that of patients without such diseases. Complete transection of the gastric corpus isolated the distal stomach from the natural pacemaker and resulted in the appearance of a new pacemaker in the distal stomach with a slower frequency. The fact that proximal gastric vagotomy did not greatly alter the frequency of generation or the pattern of propagation of the pacesetter potential provided further evidence that both are myogenic phenomena.