Topics in Compan An Med 29 (2014) 64–66
Topical Review
The Relationship Between Gastrointestinal Motility and Gastric Dilatation-Volvulus in Dogs Krista M. Gazzola, DVM, Laura L. Nelson, DVM, MS, DACVS-SAn Keywords: gastropexy motilin wireless motility device wireless motility capsule Department of Small Animal Clinical Sciences, Veterinary Medical Center, Michigan State University, East Lansing, MI, USA n
Address reprint requests to: Laura L. Nelson, DVM, MS, DACVS-SA, Department of Small Animal Clinical Sciences, Veterinary Medical Center, Michigan State University, 736 Wilson Road, Room D211, East Lansing, MI 48824, USA.
Gastric dilatation-volvulus (GDV) is a devastating disease that most commonly affects large and giantbreed dogs. Though a number of risk factors have been associated with the development of GDV, the etiology of GDV remains unclear. Abnormal gastric motility patterns and delayed gastric emptying have been previously described in dogs following GDV. Work evaluating the effects of gastropexy procedures and changes to gastric motility after experimental GDV has not found the same changes as those found in dogs with naturally occurring GDV. Although the role of abnormal gastric motility in dogs with GDV will need to be clarified with additional research, such study is likely to be facilitated by improved access to and development of noninvasive measurement techniques for the evaluation of gastric emptying and other motility parameters. In particular, the availability of Food and Drug Administration–approved wireless motility devices for the evaluation of gastrointestinal motility is particularly promising in the study of GDV and other functional gastrointestinal diseases of large and giant-breed dogs. Published by Elsevier Inc.
E-mail: [email protected] (L.L. Nelson)
Gastric dilatation-volvulus (GDV) is a devastating and often deadly disease affecting primarily large and giant-breed dogs. This condition is characterized by rotation of the stomach around its axis, trapping air within the gastric lumen and increasing intragastric pressure. An increase in intragastric pressure causes a subsequent decrease in venous flow through the abdomen via direct compression. The consequence of this is a life-threatening combination of portal hypertension, systemic hypotension, and shock.1 The reported lifetime risk for specific dogs predisposed to the development of GDV is estimated to be between 4% and 37%.2 Breeds considered to be at the highest risk include Great Danes, Gordon Setters, Irish Setters, Weimaraners, Saint Bernards, Standard Poodles, and Bassett Hounds.1 The underlying cause of GDV is not well understood. There are many factors associated with increased GDV risk, including increasing age, underweight body condition, a history of GDV in a first-degree relative, eating rapidly, once-daily feedings, fearful or anxious temperament, and an increased thoracic depth-width ratio.3,4 It should be noted that these associated risk factors have not been shown to cause GDV, but they suggest a strong likelihood of a genetic link. It has also been established that dogs with GDV have abnormalities in gastrointestinal motility that cannot be explained by gastropexy or dilation alone.5 The goals of this article are to review normal gastrointestinal motility in dogs, to discuss the conclusions of previous research on gastrointestinal motility in dogs related to the understanding and prevention of GDV, and concurrently to discuss methods for evaluating gastrointestinal motility.
Gastric Motility Gastric emptying is the process by which food is delivered to the small intestine at a rate and in a form that optimizes intestinal absorption of nutrients. The rate of gastric emptying is regulated http://dx.doi.org/10.1053/j.tcam.2014.09.006 1527-3369/& 2014 Topics in Companion Animal Medicine. Published by Elsevier Inc.
by the tonic contraction of the proximal stomach (fundus), contraction of the distal stomach (antrum), and the inhibitory forces of pyloric and duodenal contraction. Gastric emptying consists of both solid and liquid phases, with the solid phase acting as a means of mixing or trituration of solid food. During this process, food is mechanically broken down and mixed to a semiliquid chime through repeated to-and-fro movement of ingesta in the antrum. The tone of the proximal stomach plays an important role in liquid phase emptying, which is further regulated by outlet resistance from the antral and pyloric regions of the stomach and the proximal duodenum. During solid phase gastric emptying, antral contractions, characterized by the features of peristalsis (circular rings of muscular contraction), increase in amplitude and velocity as they travel distally toward the pylorus. Particles too large to pass through the pylorus ( 42 mm) are propelled back into the body of the stomach in a process termed contractile retropulsion. Contractile retropulsion reduces digestible food particles to a size suitable for gastric emptying (0.1-0.63 mm in dogs). The entire process of gastric emptying in dogs is an attempt at maintaining and recovering the interdigestive motor pattern. The interdigestive motor pattern is considered recovered when large indigestible solids have been reduced to digestible solids and gastric emptying has been completed.6 Normal fasting gastric motility in both humans and dogs is dominated by the presence of interdigestive migrating contractions (IMCs, also called migrating motor complexes).7 These are cyclic, recurring complexes of motor activity that migrate periodically from the stomach to the distal small intestine.6,7 Gastric IMCs are characterized by 3-4 distinct, cyclical phases occurring every 90-120 minutes: phase I is a quiescent period with minimal contractions; phase II contains low-amplitude mixing contractions; and phase III consists of high-amplitude, regular propulsive contractions. Phase IV, described by some groups,7 represents a short transition period back to the quiescence of phase I.6,7 These
K.M. Gazzola, L.L. Nelson / Topics in Companion An Med 29 (2014) 64–66
complexes are under hormonal control (motilin and ghrelin) with modulation by the autonomic nervous system. They serve to “cleanse” the stomach in preparation for the next meal by ensuring clearance of nondigestible solids. The duodenum, which stores motilin, plays an important role in initiating gastric migrating motor complexes in dogs and in humans, especially during gastric phase III.6,7 Gastric phase III contractions are initiated by motilin spikes and can be inhibited by stress in dogs. Stressful stimuli have been shown to reduce vagal activity and increase sympathetic tone in both humans and dogs,7 decreasing the normal maintenance of IMCs. When gastric phase III activity is impaired, material is retained in the stomach, potentially resulting in bacterial overgrowth. In humans, bacterial overgrowth has been previously proposed to be a result of motility disorders, corresponding to a diminished or absent IMCs.7 Impaired gastric IMCs may aggravate dyspeptic symptoms following the ingestion of a meal.7 Gastric Motility and GDV There has long been an association between GDV and abnormal gastric motility in dogs. However, it has been difficult to determine if the abnormalities in motility noted in dogs following GDV were a consequence of the disease or associated gastropexy or if the abnormalities were part of a progressive process that ultimately led to GDV. There is precedence in other species for abnormalities in motility to be associated with a gastric dilatation and ultimately displacement. A recent study in German Holstein cattle identified a mutation in the gene encoding motilin that was associated with an increased risk of left-sided displacement of the abomasum.8 It is possible that hypomotility leads to repeated subclinical episodes of gastric distension (bloat) that stretch gastric ligaments to the extent that the more catastrophic displacements characteristic of GDV can occur. In 1967, Funkquist and Garmer9 described decreased clearance of liquid barium from the stomach in large dogs 2 days to 2 years after surviving “acute attacks of gastric torsion.” A later report by Hall10 evaluated gastric myoelectric and motor activity using surgically placed electrodes and strain-gauge force transducers in dogs that had undergone circumcostal gastropexy (CG) as part of GDV treatment and in control dogs undergoing CG alone. In this study, electrical and mechanical activities were evaluated at 10 days following implantation before and after feeding a standardized meal. Recordings from dogs that had survived GDV and gastropexy showed increased slow-wave propagation velocity and atypical IMC fasting state phase III activity fronts when compared with normal and CG-only dogs. The study concluded that abnormalities in gastric motor activity in dogs with naturally occurring GDV are associated with GDV, not the accompanying gastropexy procedure.10 A similar study from the same laboratory used nondigestible radiopaque markers to evaluate gastric emptying time in normal dogs with and without CG and dogs following treatment for GDV and CG.11 The results of this study showed that CG did not alter the 90% gastric emptying time for radiopaque particles in healthy dogs. However, in the GDV and CG dogs, gastric emptying was significantly prolonged. These studies suggest that gastropexy procedures performed to prevent GDV recurrence are probably not the cause of postoperative gastric motility changes in dogs following GDV, but they do not address whether abnormalities in gastric motility preceded GDV.10,11 Another study sought to reproduce GDV in normal dogs through the rotation and distension of the stomach to an intragastric pressure of 30 mm Hg for 180 minutes (dogs with naturally occurring GDV have a mean gastric pressure of 22.9 mm Hg).5 Similar electrical and force transducers were used to record baseline data before and after induced GDV. Gastric electrical
65
and contractile activities were then recorded on days 1, 4, 7, and 10 postdilation. The results of this study showed no significant difference in any of the variables used to characterize gastric electrical and contractile activities, even at day 1. This suggests that differences in gastric electromechanical activity secondary to acute induced gastric dilatation are not significant.5 This study did not compare dogs undergoing naturally occurring GDV in the same way, but it suggests that the distension and displacement of the stomach alone do not explain the abnormalities noted in dogs following GDV. A 2013 study evaluating the efficacy of incisional gastropexy (IG) in the prevention of GDV in dogs reported a recurrence rate of 0%.3 The same study noted that gastric dilatation without volvulus occurred in dogs that underwent the procedure prophylactically and in some dogs that underwent the procedure as part of GDV treatment, with rates of 11.1% and 8.8%, respectively. Because previous research suggests that gastropexy alone does not have a significant negative effect on gastric motility, the occurrence of gastric dilatation without volvulus in dogs after IG alone suggests that these dogs, likely predisposed to GDV based on breed and family history, are exhibiting abnormalities in gastric motility that may be similar to dogs following GDV. It should be noted that, unlike CG, the effects of IG on gastric motility have not been evaluated and that further evaluation of the effects of IG on motility are warranted based on the widespread prophylactic use of the technique.3,11 A variety of tests have been used in the assessment of gastrointestinal motility in these studies. Although some of these tests, such as contrast radiography, are noninvasive and appropriate for clinical use, others are invasive and more limited to research applications. These and other techniques for the assessment of gastric emptying and other parameters relating to gastrointestinal motility are summarized in the following sections.
Assessment of Gastric Motility The evaluation of gastric motility in dogs before and after GDV is complicated by a number of factors. First of all, the complexity of gastrointestinal motility alters parameters such as gastric emptying time potentially by factors such as stress due to hospitalization or travel, fasting vs. fed state, concurrent medication or anesthetics, and individual variation. Additionally, there is limited information about changes in gastrointestinal motility in the diseased animal. Finally, the most common means of evaluating gastric motility in dogs have limitations. The ideal means of measuring gastric motility would be quantifiable, repeatable, noninvasive, practical, and not stressful to the patient. Methods described for the assessment of gastrointestinal motility and emptying have included imaging methods, tracer studies, measurements of electrical resistance, and more recently, wireless motility devices (WMD). A brief overview of the modalities that have been employed to evaluate gastrointestinal motility in dogs following naturally occurring or experimental GDV is given in the following sections. Many of these methods have been described elsewhere in greater detail.6 Contrast radiography involves sequential lateral and ventrodorsal images obtained following the ingestion of a radio-opaque meal. Radio-opaque materials include liquid barium, barium mixed with food, and radio-opaque indigestible solids or markers. Because these materials are not similar to food and often require force feeding or tube feeding for administration, it is difficult to accurately assess the subtle modulations in the rate of gastric emptying. This method is best suited for gross abnormalities that would be associated with delayed gastric emptying, such as a functional or mechanical obstruction. This method most easily
66
K.M. Gazzola, L.L. Nelson / Topics in Companion An Med 29 (2014) 64–66
allows assessment of a single phase of gastric emptying at a time, either liquid or solid.6,12 The advantage of this technique is the widespread availability of x-ray equipment. Radioscintigraphy can be used to determine gastric emptying after ingestion of a radionuclide-labeled meal. Commonly employed radioisotopes include technetium and indium. These radionuclides have short half-lives and, because they emit gamma radiation at different energies, they can be combined to preferentially label the solid and liquid phases of gastric emptying, allowing evaluation of both phases in a single radiolabeled meal (“dual-isotope” method). Radioscintigraphy is considered the gold standard means of evaluating gastric emptying in dogs. Disadvantages of the technique include limited availability because of the requirement for nuclear medicine facilities and use of radiation.6 Invasive techniques for evaluating gastric myoelectric and motor activity in dogs have been described using surgically implanted electrodes and strain-gauge force transducers.10,11 Though valuable, these techniques are less practical in the evaluation of clinical patients. Tracer studies can involve gastric tracers, plasma tracers, or breath tracers. Breath tracers allow assessment of gastric emptying by stable isotope breath tests involving ingestion of a C-labeled substrate that is rapidly absorbed and metabolized to CO2.12 Breath tracer 13C-sodium acetate, specifically, has been used recently to evaluate gastric emptying times in normal dogs, dogs following non-GDV abdominal surgery, and in dogs following surgery for GDV. It can be considered a validated and minimally invasive test that could prove to be helpful in a clinical setting.6,12 WMD (also called wireless motility capsules) have been of recent interest as a noninvasive, practical means of assessing gastric emptying in dogs.13 WMD have been assessed in dogs, demonstrating repeatability of measurement equivalent to that obtained by the use of scintigraphy.13,14 A commercially available WMD (SmartPill, Given Imaging Inc., Duluth, GA) is a 26-mm 13-mm capsule that contains sensors for the measurement of pressure, temperature, and pH. The capsule is administered orally to the patient, and then transmits data wirelessly to a small receiver worn by the patient. After data are transferred to a computer, an interpretation software (MotiliGI, Given Imaging Inc., Duluth, GA) allows the quantitative interpretation of motility data. This device is used in the evaluation and diagnosis of gastroparesis, functional dyspepsia, and chronic constipation in humans. In comparison with other means of evaluating gastric motility or gastric emptying time, WMD are noninvasive, provide quantitative data, and do not involve radioisotopes, hospitalization, or physical restraint. Additionally, this technology can be utilized at home to minimize patient stress.
Future Directions, Clinical Significance and Conclusions Despite a large body of literature evaluating risk factors, treatment, and preventive procedures, the underlying cause of GDV in most dogs remains obscure. With improvements in the assessment of gastrointestinal motility, further evaluation of the role of
gastric motility in the development of and recovery from GDV is indicated. If similar abnormalities are identified in dogs predisposed to GDV based on breed and family history and in dogs that have survived GDV, a causative relationship between abnormal motility and GDV might be inferred and further evaluated. In addition, such information would allow researchers to investigate the etiology of the abnormality, facilitating treatment or prophylactic gastropexy for affected dogs. If such an abnormality is determined to be heritable, screening tests may be developed to help breeders to reduce the expression of this trait in their lines, potentially reducing the effect of this devastating disease.
Acknowledgments The authors would like to acknowledge the Michigan State University College of Veterinary Medicine Endowed Research Fund and American Kennel Club Canine Health Foundation for supporting current and future research in this area. References 1. Tobias KM, Johnston SA, editors. Veterinary Surgery: Small Animal. Saunders Elsevier; 2012 2. Ward MP, Patronek GJ, Glickman LT. Benefits of prophylactic gastropexy for dogs at risk of gastric dilatation-volvulus. Prev Vet Med 60:319–329, 2003 3. Benitez ME, Schmiedt CW, Radlinsky MG, Cornell KK. Efficacy of incisional gastropexy for the prevention of GDV in dogs. J Am Anim Hosp Assoc 49:185–189, 2013 4. Raghavan M, Glickman N, McGabe G, Lantz G, Glickman LT. Diet-related risk factors for gastric dilatation-volvulus in dogs of high-risk breeds. J Am Animal Hosp Assoc 40:192–203, 2004 5. Stampley AR, Burrows CF, Ellison GW, Tooker J. Gastric myoelectric activity after experimental gastric dilatation-volvulus and tube gastrostomy in dogs. Vet Surg 21:10–14, 1992 6. Wyse CA, McLellan J, Dickie AM, Sutton DG, Preston T, Yam PS. A review of methods for assessment of gastric empyting in the dog and cat: 1989-2002. J Vet Intern Med 17:609–621, 2003 7. Takahashi T. Mechanism of interdigestive migrating motor complex. J Neurogastroenterol Motil 18:246–257, 2012 8. Momke S, Sickinger M, Rehage J, Doll K, Distl O. Transcription factor binding site polymorphism in the Motilin gene associated with left-sided displacement of the abomasums in German Holstein cattle. PLoS One 12:e35562, 2012 9. Funkquist B, Garmer L. Pathogenic and therapeutic aspects of torsion of the canine stomach. J Small Anim Pract 8:523–532, 1967 10. Hall JA: Gastric Myoelectric and Motor Activity in Normal Dogs and Dogs With Gastric Dilatation-Volvulus. [PhD Dissertation]. Ft. Collins, CO: Colorado State Univesity, 1989 11. Hall JA, Willer RL, Solie TN, Twedt DC. Effect of circumcostal gastropexy on gastric myoelectric and motor activity in dogs. J Small Anim Pract 38:200–207, 1997 12. Schmitz S, Jansen N, Failing K, Neiger R. 13C-sodium acetate breath test for evaluation of gastric emptying times in dogs with gastric dilatation-volvulus. Tierarztl Prax Ausq K Kleintiere Heimtiere 2:87–92, 2013 13. Lidbury JA, Suchodolski JS, Ivanek R, Steiner JM. Assessment of the variation associated with repeated measurement of gastrointestinal transit times and assessment of the effect of oral ranitidine on gastrointestinal transit times using a wireless motility capsule system in dogs. Vet Med Int; 2012(Article ID 938417, 8 pages) 14. Boillat CS, Gaschen FP, Gaschen L, Stout RW, Hosgood GL. Variability associated with repeated measurements of gastrointestinal tract motility in dogs obtained by use of a wireless motility capsule system and scintigraphy. Am J Vet Res 8:903–908, 2010
Topical Review
The Relationship Between Gastrointestinal Motility and Gastric Dilatation-Volvulus in Dogs Krista M. Gazzola, DVM, Laura L. Nelson, DVM, MS, DACVS-SAn Keywords: gastropexy motilin wireless motility device wireless motility capsule Department of Small Animal Clinical Sciences, Veterinary Medical Center, Michigan State University, East Lansing, MI, USA n
Address reprint requests to: Laura L. Nelson, DVM, MS, DACVS-SA, Department of Small Animal Clinical Sciences, Veterinary Medical Center, Michigan State University, 736 Wilson Road, Room D211, East Lansing, MI 48824, USA.
Gastric dilatation-volvulus (GDV) is a devastating disease that most commonly affects large and giantbreed dogs. Though a number of risk factors have been associated with the development of GDV, the etiology of GDV remains unclear. Abnormal gastric motility patterns and delayed gastric emptying have been previously described in dogs following GDV. Work evaluating the effects of gastropexy procedures and changes to gastric motility after experimental GDV has not found the same changes as those found in dogs with naturally occurring GDV. Although the role of abnormal gastric motility in dogs with GDV will need to be clarified with additional research, such study is likely to be facilitated by improved access to and development of noninvasive measurement techniques for the evaluation of gastric emptying and other motility parameters. In particular, the availability of Food and Drug Administration–approved wireless motility devices for the evaluation of gastrointestinal motility is particularly promising in the study of GDV and other functional gastrointestinal diseases of large and giant-breed dogs. Published by Elsevier Inc.
E-mail: [email protected] (L.L. Nelson)
Gastric dilatation-volvulus (GDV) is a devastating and often deadly disease affecting primarily large and giant-breed dogs. This condition is characterized by rotation of the stomach around its axis, trapping air within the gastric lumen and increasing intragastric pressure. An increase in intragastric pressure causes a subsequent decrease in venous flow through the abdomen via direct compression. The consequence of this is a life-threatening combination of portal hypertension, systemic hypotension, and shock.1 The reported lifetime risk for specific dogs predisposed to the development of GDV is estimated to be between 4% and 37%.2 Breeds considered to be at the highest risk include Great Danes, Gordon Setters, Irish Setters, Weimaraners, Saint Bernards, Standard Poodles, and Bassett Hounds.1 The underlying cause of GDV is not well understood. There are many factors associated with increased GDV risk, including increasing age, underweight body condition, a history of GDV in a first-degree relative, eating rapidly, once-daily feedings, fearful or anxious temperament, and an increased thoracic depth-width ratio.3,4 It should be noted that these associated risk factors have not been shown to cause GDV, but they suggest a strong likelihood of a genetic link. It has also been established that dogs with GDV have abnormalities in gastrointestinal motility that cannot be explained by gastropexy or dilation alone.5 The goals of this article are to review normal gastrointestinal motility in dogs, to discuss the conclusions of previous research on gastrointestinal motility in dogs related to the understanding and prevention of GDV, and concurrently to discuss methods for evaluating gastrointestinal motility.
Gastric Motility Gastric emptying is the process by which food is delivered to the small intestine at a rate and in a form that optimizes intestinal absorption of nutrients. The rate of gastric emptying is regulated http://dx.doi.org/10.1053/j.tcam.2014.09.006 1527-3369/& 2014 Topics in Companion Animal Medicine. Published by Elsevier Inc.
by the tonic contraction of the proximal stomach (fundus), contraction of the distal stomach (antrum), and the inhibitory forces of pyloric and duodenal contraction. Gastric emptying consists of both solid and liquid phases, with the solid phase acting as a means of mixing or trituration of solid food. During this process, food is mechanically broken down and mixed to a semiliquid chime through repeated to-and-fro movement of ingesta in the antrum. The tone of the proximal stomach plays an important role in liquid phase emptying, which is further regulated by outlet resistance from the antral and pyloric regions of the stomach and the proximal duodenum. During solid phase gastric emptying, antral contractions, characterized by the features of peristalsis (circular rings of muscular contraction), increase in amplitude and velocity as they travel distally toward the pylorus. Particles too large to pass through the pylorus ( 42 mm) are propelled back into the body of the stomach in a process termed contractile retropulsion. Contractile retropulsion reduces digestible food particles to a size suitable for gastric emptying (0.1-0.63 mm in dogs). The entire process of gastric emptying in dogs is an attempt at maintaining and recovering the interdigestive motor pattern. The interdigestive motor pattern is considered recovered when large indigestible solids have been reduced to digestible solids and gastric emptying has been completed.6 Normal fasting gastric motility in both humans and dogs is dominated by the presence of interdigestive migrating contractions (IMCs, also called migrating motor complexes).7 These are cyclic, recurring complexes of motor activity that migrate periodically from the stomach to the distal small intestine.6,7 Gastric IMCs are characterized by 3-4 distinct, cyclical phases occurring every 90-120 minutes: phase I is a quiescent period with minimal contractions; phase II contains low-amplitude mixing contractions; and phase III consists of high-amplitude, regular propulsive contractions. Phase IV, described by some groups,7 represents a short transition period back to the quiescence of phase I.6,7 These
K.M. Gazzola, L.L. Nelson / Topics in Companion An Med 29 (2014) 64–66
complexes are under hormonal control (motilin and ghrelin) with modulation by the autonomic nervous system. They serve to “cleanse” the stomach in preparation for the next meal by ensuring clearance of nondigestible solids. The duodenum, which stores motilin, plays an important role in initiating gastric migrating motor complexes in dogs and in humans, especially during gastric phase III.6,7 Gastric phase III contractions are initiated by motilin spikes and can be inhibited by stress in dogs. Stressful stimuli have been shown to reduce vagal activity and increase sympathetic tone in both humans and dogs,7 decreasing the normal maintenance of IMCs. When gastric phase III activity is impaired, material is retained in the stomach, potentially resulting in bacterial overgrowth. In humans, bacterial overgrowth has been previously proposed to be a result of motility disorders, corresponding to a diminished or absent IMCs.7 Impaired gastric IMCs may aggravate dyspeptic symptoms following the ingestion of a meal.7 Gastric Motility and GDV There has long been an association between GDV and abnormal gastric motility in dogs. However, it has been difficult to determine if the abnormalities in motility noted in dogs following GDV were a consequence of the disease or associated gastropexy or if the abnormalities were part of a progressive process that ultimately led to GDV. There is precedence in other species for abnormalities in motility to be associated with a gastric dilatation and ultimately displacement. A recent study in German Holstein cattle identified a mutation in the gene encoding motilin that was associated with an increased risk of left-sided displacement of the abomasum.8 It is possible that hypomotility leads to repeated subclinical episodes of gastric distension (bloat) that stretch gastric ligaments to the extent that the more catastrophic displacements characteristic of GDV can occur. In 1967, Funkquist and Garmer9 described decreased clearance of liquid barium from the stomach in large dogs 2 days to 2 years after surviving “acute attacks of gastric torsion.” A later report by Hall10 evaluated gastric myoelectric and motor activity using surgically placed electrodes and strain-gauge force transducers in dogs that had undergone circumcostal gastropexy (CG) as part of GDV treatment and in control dogs undergoing CG alone. In this study, electrical and mechanical activities were evaluated at 10 days following implantation before and after feeding a standardized meal. Recordings from dogs that had survived GDV and gastropexy showed increased slow-wave propagation velocity and atypical IMC fasting state phase III activity fronts when compared with normal and CG-only dogs. The study concluded that abnormalities in gastric motor activity in dogs with naturally occurring GDV are associated with GDV, not the accompanying gastropexy procedure.10 A similar study from the same laboratory used nondigestible radiopaque markers to evaluate gastric emptying time in normal dogs with and without CG and dogs following treatment for GDV and CG.11 The results of this study showed that CG did not alter the 90% gastric emptying time for radiopaque particles in healthy dogs. However, in the GDV and CG dogs, gastric emptying was significantly prolonged. These studies suggest that gastropexy procedures performed to prevent GDV recurrence are probably not the cause of postoperative gastric motility changes in dogs following GDV, but they do not address whether abnormalities in gastric motility preceded GDV.10,11 Another study sought to reproduce GDV in normal dogs through the rotation and distension of the stomach to an intragastric pressure of 30 mm Hg for 180 minutes (dogs with naturally occurring GDV have a mean gastric pressure of 22.9 mm Hg).5 Similar electrical and force transducers were used to record baseline data before and after induced GDV. Gastric electrical
65
and contractile activities were then recorded on days 1, 4, 7, and 10 postdilation. The results of this study showed no significant difference in any of the variables used to characterize gastric electrical and contractile activities, even at day 1. This suggests that differences in gastric electromechanical activity secondary to acute induced gastric dilatation are not significant.5 This study did not compare dogs undergoing naturally occurring GDV in the same way, but it suggests that the distension and displacement of the stomach alone do not explain the abnormalities noted in dogs following GDV. A 2013 study evaluating the efficacy of incisional gastropexy (IG) in the prevention of GDV in dogs reported a recurrence rate of 0%.3 The same study noted that gastric dilatation without volvulus occurred in dogs that underwent the procedure prophylactically and in some dogs that underwent the procedure as part of GDV treatment, with rates of 11.1% and 8.8%, respectively. Because previous research suggests that gastropexy alone does not have a significant negative effect on gastric motility, the occurrence of gastric dilatation without volvulus in dogs after IG alone suggests that these dogs, likely predisposed to GDV based on breed and family history, are exhibiting abnormalities in gastric motility that may be similar to dogs following GDV. It should be noted that, unlike CG, the effects of IG on gastric motility have not been evaluated and that further evaluation of the effects of IG on motility are warranted based on the widespread prophylactic use of the technique.3,11 A variety of tests have been used in the assessment of gastrointestinal motility in these studies. Although some of these tests, such as contrast radiography, are noninvasive and appropriate for clinical use, others are invasive and more limited to research applications. These and other techniques for the assessment of gastric emptying and other parameters relating to gastrointestinal motility are summarized in the following sections.
Assessment of Gastric Motility The evaluation of gastric motility in dogs before and after GDV is complicated by a number of factors. First of all, the complexity of gastrointestinal motility alters parameters such as gastric emptying time potentially by factors such as stress due to hospitalization or travel, fasting vs. fed state, concurrent medication or anesthetics, and individual variation. Additionally, there is limited information about changes in gastrointestinal motility in the diseased animal. Finally, the most common means of evaluating gastric motility in dogs have limitations. The ideal means of measuring gastric motility would be quantifiable, repeatable, noninvasive, practical, and not stressful to the patient. Methods described for the assessment of gastrointestinal motility and emptying have included imaging methods, tracer studies, measurements of electrical resistance, and more recently, wireless motility devices (WMD). A brief overview of the modalities that have been employed to evaluate gastrointestinal motility in dogs following naturally occurring or experimental GDV is given in the following sections. Many of these methods have been described elsewhere in greater detail.6 Contrast radiography involves sequential lateral and ventrodorsal images obtained following the ingestion of a radio-opaque meal. Radio-opaque materials include liquid barium, barium mixed with food, and radio-opaque indigestible solids or markers. Because these materials are not similar to food and often require force feeding or tube feeding for administration, it is difficult to accurately assess the subtle modulations in the rate of gastric emptying. This method is best suited for gross abnormalities that would be associated with delayed gastric emptying, such as a functional or mechanical obstruction. This method most easily
66
K.M. Gazzola, L.L. Nelson / Topics in Companion An Med 29 (2014) 64–66
allows assessment of a single phase of gastric emptying at a time, either liquid or solid.6,12 The advantage of this technique is the widespread availability of x-ray equipment. Radioscintigraphy can be used to determine gastric emptying after ingestion of a radionuclide-labeled meal. Commonly employed radioisotopes include technetium and indium. These radionuclides have short half-lives and, because they emit gamma radiation at different energies, they can be combined to preferentially label the solid and liquid phases of gastric emptying, allowing evaluation of both phases in a single radiolabeled meal (“dual-isotope” method). Radioscintigraphy is considered the gold standard means of evaluating gastric emptying in dogs. Disadvantages of the technique include limited availability because of the requirement for nuclear medicine facilities and use of radiation.6 Invasive techniques for evaluating gastric myoelectric and motor activity in dogs have been described using surgically implanted electrodes and strain-gauge force transducers.10,11 Though valuable, these techniques are less practical in the evaluation of clinical patients. Tracer studies can involve gastric tracers, plasma tracers, or breath tracers. Breath tracers allow assessment of gastric emptying by stable isotope breath tests involving ingestion of a C-labeled substrate that is rapidly absorbed and metabolized to CO2.12 Breath tracer 13C-sodium acetate, specifically, has been used recently to evaluate gastric emptying times in normal dogs, dogs following non-GDV abdominal surgery, and in dogs following surgery for GDV. It can be considered a validated and minimally invasive test that could prove to be helpful in a clinical setting.6,12 WMD (also called wireless motility capsules) have been of recent interest as a noninvasive, practical means of assessing gastric emptying in dogs.13 WMD have been assessed in dogs, demonstrating repeatability of measurement equivalent to that obtained by the use of scintigraphy.13,14 A commercially available WMD (SmartPill, Given Imaging Inc., Duluth, GA) is a 26-mm 13-mm capsule that contains sensors for the measurement of pressure, temperature, and pH. The capsule is administered orally to the patient, and then transmits data wirelessly to a small receiver worn by the patient. After data are transferred to a computer, an interpretation software (MotiliGI, Given Imaging Inc., Duluth, GA) allows the quantitative interpretation of motility data. This device is used in the evaluation and diagnosis of gastroparesis, functional dyspepsia, and chronic constipation in humans. In comparison with other means of evaluating gastric motility or gastric emptying time, WMD are noninvasive, provide quantitative data, and do not involve radioisotopes, hospitalization, or physical restraint. Additionally, this technology can be utilized at home to minimize patient stress.
Future Directions, Clinical Significance and Conclusions Despite a large body of literature evaluating risk factors, treatment, and preventive procedures, the underlying cause of GDV in most dogs remains obscure. With improvements in the assessment of gastrointestinal motility, further evaluation of the role of
gastric motility in the development of and recovery from GDV is indicated. If similar abnormalities are identified in dogs predisposed to GDV based on breed and family history and in dogs that have survived GDV, a causative relationship between abnormal motility and GDV might be inferred and further evaluated. In addition, such information would allow researchers to investigate the etiology of the abnormality, facilitating treatment or prophylactic gastropexy for affected dogs. If such an abnormality is determined to be heritable, screening tests may be developed to help breeders to reduce the expression of this trait in their lines, potentially reducing the effect of this devastating disease.
Acknowledgments The authors would like to acknowledge the Michigan State University College of Veterinary Medicine Endowed Research Fund and American Kennel Club Canine Health Foundation for supporting current and future research in this area. References 1. Tobias KM, Johnston SA, editors. Veterinary Surgery: Small Animal. Saunders Elsevier; 2012 2. Ward MP, Patronek GJ, Glickman LT. Benefits of prophylactic gastropexy for dogs at risk of gastric dilatation-volvulus. Prev Vet Med 60:319–329, 2003 3. Benitez ME, Schmiedt CW, Radlinsky MG, Cornell KK. Efficacy of incisional gastropexy for the prevention of GDV in dogs. J Am Anim Hosp Assoc 49:185–189, 2013 4. Raghavan M, Glickman N, McGabe G, Lantz G, Glickman LT. Diet-related risk factors for gastric dilatation-volvulus in dogs of high-risk breeds. J Am Animal Hosp Assoc 40:192–203, 2004 5. Stampley AR, Burrows CF, Ellison GW, Tooker J. Gastric myoelectric activity after experimental gastric dilatation-volvulus and tube gastrostomy in dogs. Vet Surg 21:10–14, 1992 6. Wyse CA, McLellan J, Dickie AM, Sutton DG, Preston T, Yam PS. A review of methods for assessment of gastric empyting in the dog and cat: 1989-2002. J Vet Intern Med 17:609–621, 2003 7. Takahashi T. Mechanism of interdigestive migrating motor complex. J Neurogastroenterol Motil 18:246–257, 2012 8. Momke S, Sickinger M, Rehage J, Doll K, Distl O. Transcription factor binding site polymorphism in the Motilin gene associated with left-sided displacement of the abomasums in German Holstein cattle. PLoS One 12:e35562, 2012 9. Funkquist B, Garmer L. Pathogenic and therapeutic aspects of torsion of the canine stomach. J Small Anim Pract 8:523–532, 1967 10. Hall JA: Gastric Myoelectric and Motor Activity in Normal Dogs and Dogs With Gastric Dilatation-Volvulus. [PhD Dissertation]. Ft. Collins, CO: Colorado State Univesity, 1989 11. Hall JA, Willer RL, Solie TN, Twedt DC. Effect of circumcostal gastropexy on gastric myoelectric and motor activity in dogs. J Small Anim Pract 38:200–207, 1997 12. Schmitz S, Jansen N, Failing K, Neiger R. 13C-sodium acetate breath test for evaluation of gastric emptying times in dogs with gastric dilatation-volvulus. Tierarztl Prax Ausq K Kleintiere Heimtiere 2:87–92, 2013 13. Lidbury JA, Suchodolski JS, Ivanek R, Steiner JM. Assessment of the variation associated with repeated measurement of gastrointestinal transit times and assessment of the effect of oral ranitidine on gastrointestinal transit times using a wireless motility capsule system in dogs. Vet Med Int; 2012(Article ID 938417, 8 pages) 14. Boillat CS, Gaschen FP, Gaschen L, Stout RW, Hosgood GL. Variability associated with repeated measurements of gastrointestinal tract motility in dogs obtained by use of a wireless motility capsule system and scintigraphy. Am J Vet Res 8:903–908, 2010
