The esophagus is a highly distensible tube that

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1 J Vet Intern Med 2006;20: Esophageal Dysmotility in Young Dogs N.H. Bexfield, P.J. Watson, and M.E. Herrtage Background: Abnormal esophageal motility can exist without megaesophagus, although its prevalence in dogs is unknown and its cause has not been elucidated. Hypothesis: Esophageal dysmotility without overt megaesophagus exists in both symptomatic and asymptomatic young dogs, and motility can improve with age. Animals: Dogs examined at the Department of Veterinary Medicine, University of Cambridge for regurgitation, but without evidence of megaesophagus on radiographs, and a further group of asymptomatic dogs. Methods: Dogs underwent an initial and a repeat videofluoroscopic swallowing study. Images were reviewed and 5 criteria of esophageal motility evaluated. Results: Eight affected dogs were identified (median age 9 months), and terrier dogs predominated (6 terriers of 3 breeds). Esophageal motility was reduced either globally (n 5 3) or segmentally (n 5 5). Repeat examination at a median of 3 months revealed that regurgitation had reduced or resolved in the majority of terrier dogs, and 4 of 6 cases demonstrated an improvement in esophageal motility. Videofluoroscopic evaluation of young (median age 11 months) asymptomatic dogs of various breeds (n 5 22) revealed evidence of esophageal dysmotility in 4 of 5 control terrier dogs. Repeat evaluation demonstrated an improvement in esophageal motility in 3 dogs. Conclusion and Clinical Importance: Esophageal dysmotility without overt megaesophagus occurs in young terrier dogs, and affected animals can be symptomatic or asymptomatic. Further, an improvement in esophageal motility occurs with time in some dogs, and might represent a syndrome of delayed esophageal maturation. Key words: Esophagitis; Esophagus; Maturation; Megaesophagus; Motility. The esophagus is a highly distensible tube that transports ingesta from the oropharynx to the stomach. The entire length of the esophagus in dogs is striated muscle, and is innervated by the vagus nerve. 1 High pressure zones are maintained by the cranial and caudal esophageal sphincters ensuring unidirectional flow between the oropharynx and stomach. The esophageal phase of swallowing begins with relaxation of the cranial sphincter, allowing movement of a bolus into the proximal esophagus. 2 The primary peristaltic wave generated in the pharynx is propagated through the esophagus and carries the bolus aborally. If this wave fades before the bolus of food reaches the stomach, a secondary peristaltic wave is generated by intraluminal distension to complete the transport of food to the stomach. Relaxation of the caudal esophageal sphincter then allows the bolus to pass into the stomach. Megaesophagus is the most common cause of regurgitation in dogs, and the most frequently reported motility disorder to affect the canine esophagus. 2 Megaesophagus involves the loss of esophageal motor function and is characterized by ineffective esophageal peristalsis, esophageal dilation, and regurgitation. 3 Abnormal esophageal motility can occur without megaesophagus. Esophageal motor disorders are poorly defined and infrequently recognized in dogs, although there is a high prevalence of subclinical esophageal motility abnormalities reported in certain breeds such as the Chinese Shar Pei and Bouvier des Flandres. 4,5 Causes From the Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom. Reprint requests: Nick Bexfield, BVetMed, DSAM, MRCVS, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge CB3 0ES; nb289@cam.ac.uk. Received January 13, 2006; Revised April 14, 2006; Accepted April 22, Copyright E 2006 by the American College of Veterinary Internal Medicine /06/ /$3.00/0 of esophageal motility abnormalities are thought to be similar to those of megaesophagus. Indeed, it is possible that many cases of megaesophagus are preceded by a period in which esophageal motility is disrupted but esophageal dilation is yet to develop. 6 Delayed maturation of esophageal function in human infants is a relatively common cause of swallowing dysfunction, and the human esophagus can mature up to 1 year of age. 7 Similarly, the esophagus in dogs can mature up to 1 year of age. 8 The aim of this study was to document clinically significant esophageal dysmotility in dogs without overt megaesophagus. As the dogs identified were all young, a further study was undertaken to ascertain the prevalence of asymptomatic esophageal dysmotility in a young control population. Materials and Methods Between January 2000 and August 2004, clinical cases presenting to the Department of Veterinary Medicine, University of Cambridge with regurgitation but without megaesophagus on radiographs, underwent fluoroscopy. Fluoroscopy was performed according to the following standard protocol, using an image intensifier a, and recorded on video. Dogs were fasted for a minimum of 6 hours before the investigation, and fluoroscopy performed with the animal standing on 4 legs, and observed by one of the authors. A semi-moist canned food mixed with a proportionate amount of barium sulphate suspension b equivalent to approximately 10% of the total food volume was fed. Both the food and barium sulphate were stored and subsequently fed at room temperature. Four cases were lightly sedated using intramuscular acepromazine c and buprenorphine d approximately 30 minutes before fluoroscopy. The entire length of the esophagus was observed, and several boluses of food were sequentially followed. As part of the investigative procedure, all cases underwent thoracic radiography, abdominal radiography, routine CBC and serum biochemistry were also performed. Other ancillary tests including acetylcholine receptor antibody titre (n 5 8), ACTH stimulation test (n 5 2), and endoscopy (n 5 3) were also performed.

2 Esophageal Dysmotility in Dogs 1315 After the initial fluoroscopic evaluation, dogs with evidence of esophageal dysmotility had a 2nd fluoroscopic examination, if the dogs were available. A similar protocol was used as in the initial study, and dogs sedated for initial fluoroscopy were again sedated using an equal or greater dose of sedative. In addition, a study of healthy young dogs (,24 months) owned by staff and clients was undertaken, with the approval from the Ethics and Welfare Committee. All dogs underwent a fluoroscopic swallowing evaluation that was recorded on video. A standard protocol was followed, similar to that previously described, although none of these dogs were sedated. All dogs were fed the same canned food e fed at room temperature, mixed with a proportionate amount of barium sulphate suspension and examined without chemical restraint. Owners of dogs with abnormal esophageal motility were contacted approximately 3 months later and offered a 2nd fluoroscopic examination of their animal (n 5 4). All fluoroscopic images were subsequently reviewed by one of the investigators (NHB), and the criteria evaluated included: propagation distance of the primary peristaltic wave; appearance of the secondary peristaltic waves; presence of retrograde esophageal contractions; esophageal transit time; and presence of gastroesophageal reflux (GER). The propagation distance of the primary peristaltic wave was considered abnormal if it failed to move the bolus more than 5 cm into the proximal esophagus. The secondary peristaltic waves was considered abnormal if contrast material from 2 or more swallowed boluses accumulated in a portion of the esophagus causing esophageal dilation, before the stimulation of secondary peristaltic waves. Contrast retained for several seconds without stimulation of a secondary peristaltic wave was also considered abnormal, consistent with a previous study. 5 Retrograde esophageal contractions were defined as contractions moving a bolus orally over at least 10 cm of the esophagus. The esophageal phase of swallowing in control dogs with no abnormalities on fluoroscopy was complete in approximately 2 4 seconds, and was independent of body weight. Esophageal transit time was therefore considered to be prolonged when a bolus took longer than 5 seconds to reach the caudal esophageal sphincter from initiation of a primary peristaltic wave, and when other abnormalities were also present. GER was only recorded when there was clear evidence of contrast material moving from the stomach into the caudal esophagus on more than one occasion. Data are presented as median and range. Results Eight clinical cases with evidence of esophageal dysmotility on fluoroscopy were recruited to the study. Age at presentation was 9 months (2 22 months). There were 5 males and 3 females. Terrier dogs predominated (6 terriers, 2 nonterrier breeds). The terrier breeds consisted of the Border Terrier (n 5 3), West Highland White Terrier (WHWT) (n 5 2), and Manchester Terrier (n 5 1). The weights of the terrier breeds ranged from 3.8 kg to 10.9 kg (median 6.1 kg). Nonterrier breeds included a Labrador Retriever and a Rottweiler. Clinical signs were regurgitation in all dogs, and varying degrees of anorexia (n 5 5) and weight loss (n 5 4). No dog had received any medication known to be associated with esophageal disease. Six dogs had received medication before referral, including antibiotics (n 5 6), metoclopramide (n 5 3), ranitidine (n 5 2), fenbendazole (n 5 2), cimetidine (n 5 1), and sucralfate (n 5 1). No dog had a history of ingestion of irritant drugs or caustic agents or had received a general anaesthetic within the Fig 1. Freeze-frame fluoroscopic image of one of the affected dogs (4 month Border Terrier) demonstrating pooling of contrast in the proximal esophagus. This dog had segmental esophageal dysmotility. last 3 months. One dog treated with ranitidine and 1 dog treated with metoclopramide had a slight reduction in the frequency of regurgitation, but clinical signs were unchanged in the remainder of dogs. Medication had been discontinued in all dogs at least 7 days before presentation, and there had been no appreciable alteration in clinical signs in any dog. Fluoroscopic examination demonstrated abnormal esophageal motility in all cases. Esophageal motility was reduced either segmentally (n 5 5) or generally (n 5 3) (Fig 1 and 2). All dogs had more than 1 abnormality on fluoroscopy. Findings included abnormal secondary peristaltic waves (n 5 7), prolonged esophageal transit time (n 5 3), retention of contrast (n 5 2), abnormal primary peristaltic waves (n 5 1), retrograde esophageal contractions (n 5 1), and slow passage of the bolus through the caudal esophageal sphincter (n 5 1). GER was documented in 3 cases, all of which were terriers. No dog had evidence of megaesophagus on thoracic radiographs or fluoroscopy. Results of hematology and biochemistry were generally unremarkable, and demonstrated only age related changes. No abnormalities were detected by endoscopy in the 3 dogs in which it was performed. Results of acetylcholine receptor antibody tests were not diagnostic for myasthenia gravis in any of the 8 dogs, and an ACTH stimulation test was not diagnostic for hypoadrenocorticism in 2 dogs. All affected dogs were fed with their regular food, and provided with water from a height. The 5 dogs that did not undergo endoscopy were also treated for potential esophagitis with a combination of sucralfate f and ranitidine liquid g. These dogs were a Border Terrier (n 5 2), WHWT (n 5 1), Manchester Terrier (n 5 1), and Rottweiler (n 5 1). Six cases presented for re-examina-

3 1316 Bexfield, Watson, and Herrtage Fig 2. Freeze-frame fluoroscopic image of one of the affected dogs (7 month Border Terrier) demonstrating pooling of contrast in the entire portion of the visible esophagus. This dog had generalized esophageal dysmotility. tion at a median of 4 months after initial presentation (range 1K 9 months). The owner of 1 case (16 month Labrador Retriever) declined repeat examination, and reported clinical signs to be generally unchanged. The remaining case (12 month Border Terrier) was lost to follow-up. Clinical signs of regurgitation were completely resolved (n 5 3), reduced in frequency (n 5 2), or unchanged (n 5 1). Repeat fluoroscopic examination revealed esophageal motility to have improved in 4 terrier dogs, and these animals also demonstrated a reduction (n 5 1) or cessation (n 5 3) of clinical signs. These 4 terrier dogs were aged between 3 and 7 months. Changes in esophageal motility included improvement or normalization in secondary peristaltic waves (n 5 4), decrease in frequency of GER (n 5 2), and decrease in esophageal transit time (n 5 1). Improvement in secondary peristaltic waves was documented if fewer boluses accumulated in a portion of the esophagus causing esophageal dilation, before the stimulation of secondary peristaltic waves, or if there was less retention of contrast. There was no improvement in the primary peristaltic wave in the 1 dog that initially demonstrated this abnormality. Esophageal motility in the oldest dog (22 month WHWT) was unchanged, although this case demonstrated a reduction in clinical signs. In the remaining case (Rottweiler), reexamined at 9 months after initial presentation, esophageal motility had worsened and there was now evidence of GER. This case had demonstrated no improvement in clinical signs. Twenty-two young asymptomatic dogs were also recruited. All dogs were clinically healthy at the time of evaluation, and none had a previous history of regurgitation. Five terrier breeds and 17 nonterrier breeds were included. Terrier breeds included the WHWT and the Border Terrier. Nonterrier breeds included crossbreed (n 5 4), Labrador Retriever (n 5 2), German Shepherd dog (n 5 2), Greyhound (n 5 2), Border Collie (n 5 1), American Cocker Spaniel (n 5 1), Cavalier King Charles Spaniel (n 5 1), Boxer (n 5 1), English Pointer (n 5 1), Miniature Schnauzer (n 5 1), and English Bulldog (n 5 1). Age at presentation was 11 months (5 22 months). The weight of the terrier breeds ranged from 5.1 kg to 9.7 kg and that of the nonterrier breeds from 3.5 kg to 36.2 kg. Videofluoroscopic evaluation revealed evidence of esophageal dysmotility in 4 of 5 control terrier dogs, but not in any of the nonterrier breeds (n 5 17). The unaffected terrier was an 18 month old Border Terrier. Esophageal motility was reduced either generally (n 5 3) or segmentally (n 5 1) in the 4 affected terrier dogs. Findings in these dogs included abnormal secondary peristaltic waves (n 5 3), prolonged esophageal transit time (n 5 2), retention of contrast (n 5 1), abnormal primary peristaltic waves (n 5 1) and retrograde esophageal contractions (n 5 1). GER was present in 3 dogs. Although assessment was subjective, the difference between dogs with esophageal dysmotility, either clinically affected or asymptomatic controls, and asymptomatic control dogs with normal esophageal motility dogs was dramatic. Repeat fluoroscopy was performed on all 5 asymptomatic terrier dogs at a median of 3 months (range 3 5 months) after initial examination. Of the 4 dogs that previously demonstrated abnormal esophageal motility, there was an improvement in motility in 3, consisting of improved secondary peristaltic waves (n 5 3), improved esophageal tone (n 5 1), cessation of retrograde esophageal contractions (n 5 1), and cessation of GER (n 5 1). GER remained unchanged in 2 dogs, and esophageal transit time remained prolonged in the 1 dog that initially documented this abnormality. Dogs that demonstrated an improvement were aged 5, 7, and 7 months. Esophageal motility in the oldest dog (22 months) remained unchanged. Esophageal motility remained normal in 1 dog. No dog had evidence of a megaesophagus on fluoroscopy, and all dogs remained clinically normal. At the time of writing, a median of 16 months (range months) from 1st fluoroscopy, none of these dogs have developed clinical signs of esophageal dysfunction. Discussion This study documents the presence of esophageal dysmotility, without overt megaesophagus, in both symptomatic and asymptomatic dogs. It also suggests that esophageal dysmotility might be common in certain young terrier breeds, with affected animals not always demonstrating overt clinical signs. Furthermore esophageal motility appears to improve with time in some young terrier dogs. In the present study, 8 dogs were found to have clinical signs associated with fluoroscopic evidence of esophageal dysmotility, and 6 of these were terriers. All dogs demonstrated regurgitation and other signs in-

4 Esophageal Dysmotility in Dogs 1317 cluding anorexia and weight loss. Four dogs were identified in the prospective study, all of which were terriers, and had esophageal dysmotility evident on fluoroscopy. None of these dogs had clinical signs indicative of esophageal dysfunction. There are several potential causes of the esophageal dysfunction documented in the present study. Delayed maturation of esophageal function is a common cause of swallowing dysfunction in human infants, and the human esophagus can take up to 1 year after birth to fully mature. 7 Indeed nonspecific esophageal motility disorders are identified relatively commonly in young children with upper gastrointestinal symptoms. 9 Similarly, the canine esophagus can demonstrate postnatal maturation up to 1 year of age. 8 Improvement of esophageal function with age is thought to be attributed to maturation of the neuromuscular system of the esophagus. 10,11 As all terrier dogs that did show an improvement in esophageal motility were under 1 year of age, it is possible they may have been suffering from delayed esophageal maturation. The 2 terrier dogs that demonstrated no improvement in esophageal motility on re-examination were the oldest in the study (both 22 months), and therefore likely to have been fully mature. The 18-month-old control terrier had normal esophageal motility. The other case to demonstrate deterioration in esophageal motility on subsequent examination was a nonterrier breed (Rottweiler), and indeed the only nonterrier breed in the clinical cases that had follow-up fluoroscopy. The high number of affected terriers in this study that demonstrated an improvement in esophageal motility with age, may suggest delayed esophageal maturation to be common in certain terrier breeds. Unfortunately only 3 terrier breeds were represented in this study, namely the WHWT, Border Terrier, and Manchester Terrier. Further serial prospective studies of growing dogs and a wider number of terrier breeds are therefore indicated to elucidate if delayed esophageal maturation is indeed common in all terrier breeds. Esophagitis is also a particularly well-recognized cause of esophageal motility abnormalities in humans, 12 and has been described in dogs. 13 The pathogenesis of the motility disorder resulting from esophagitis is not fully understood. GER is a well documented cause of esophagitis in both humans and dogs. 2 GER describes the reflux of stomach and duodenal contents into the esophagus, and can therefore indirectly lead to esophageal dysmotility because of a resultant esophagitis. In humans, GER can be associated with a disturbed motor function within the entire upper gastrointestinal tract. 14 Two of the 3 dogs with GER in this study had esophageal dysmotility in the entire esophagus. Although there was an apparent high incidence of GER in the present study, there is intermittent GER in normal dogs. 15 The high prevalence of GER seen in terriers in this study might play a role in the development of esophageal dysmotility. Ideally diagnostic testing and treatment would have been standardized in all clinical cases, but regrettably this was not possible, and was dictated by financial and owner constraints. Treatment of the clinical cases was generally similar to that of megaesophagus. Animals were managed by feeding and providing water from an elevated position. All dogs were fed their regular food, although the composition was adjusted for the particular patient, as some animals show fewer clinical signs when solid, rather than liquid, food is fed. Three clinical cases with esophageal dysmotility underwent esophagoscopy in an attempt to diagnose esophagitis. In the remaining 5 dogs, therapy for potential esophagitis was initiated. Three out of 5 cases treated for esophagitis, all young terriers, did demonstrate an improvement in esophageal motility and clinical signs on re-examination, although motility still appeared abnormal on fluoroscopy. In addition, one young terrier not treated for esophagitis also demonstrated an improvement in esophageal motility. It is possible that esophageal motility improved in these dogs as a result of therapy for esophagitis. The improvement in both clinical cases treated and untreated for esophagitis, suggests that esophagitis was less likely to be a cause of the abnormal esophageal motility. In addition, the fact that motility did not completely return to normal, suggests that the abnormal esophageal motor function was not entirely due to esophagitis or that the damage caused was irreversible. Although no underlying cause of the esophageal motility abnormalities was identified in any animal, not all symptomatic animals underwent a complete diagnostic evaluation, hence the term idiopathic can not be applied to all cases. Asymptomatic animals with esophageal dysmotility were not evaluated for presence of underlying diseases, nor were acetylcholine receptor antibodies measured in this group of animals. These animals were healthy at the time of evaluation, and had no clinical signs to suggest concurrent disease. It is possible however, that all or some of these animals may have had an underlying disease responsible for esophageal dysmotility. Previous studies in dogs have demonstrated that in some cases, megaesophagus appears to be preceded by a period in which esophageal motility is deranged but esophageal dilation has not yet developed. 2,6 However, there was no evidence of esophageal dysmotility progressing to megaesophagus in the dogs in the present study, because repeat fluoroscopic examination generally demonstrated an improvement in motility with time. None of the clinical cases demonstrated evidence of megaesophagus on fluoroscopy at re-examination. Thoracic radiography was not performed in the control dogs to document the presence of megaesophagus. Because all of the control dogs are still asymptomatic at the time of writing this suggests it is unlikely that these dogs have progressed to overt megaesophagus. Esophageal motility in the present study was assessed using fluoroscopy, with some criteria based on previous studies of normal function. 5,15 Because of a relative paucity of information available in the literature on the fluoroscopic appearance of esophageal motility, several additional criteria were used in an attempt to make assessment as objective as possible. Importantly, the

5 1318 Bexfield, Watson, and Herrtage objective criteria allowed comparison among different animals. The authors accept however, that despite their efforts to make this study as objective as possible, some subjectivity may still remain. An increased incidence of esophageal foreign bodies in terrier breeds has been reported previously. 16,17 In both studies over 50% of affected dogs were terriers, although their ages were not reported. Esophageal dysmotility may be a contributing factor to the high incidence of esophageal foreign bodies in this breed type. A relatively high occurrence of both clinically apparent and subclinical esophageal dysmotility was found in certain young terrier breeds compared with nonterrier breeds, which may represent a syndrome of delayed esophageal maturation. A number of terrier dogs also exhibited GER, and we postulate that these animals may develop esophagitis, leading to the development of esophageal dysmotility. Further studies are indicated in larger numbers of terrier breeds to assess the true incidence of esophageal dysmotility in these breeds. Footnotes a Stenoscop, General Electric Medical Systems Ltd, Loncin, Belgium b Polibar Rapid 100.6% w/v, Ezem Ltd, Bicester, Oxfordshire, UK c ACP, Novartis Animal Health, Litlington, Herts, UK d Vetergesic, Alstoe Animal Health, York, North Yorkshire, UK e Sensitivity Control, Royal Canin, Yeovil, Somerset, UK f Antepsin oral suspension, Chugai Pharma Ltd, Turnham Green, London, UK g Zantac syrup, GlaxoSmithKline, Uxbridge, Middlesex, UK Acknowledgments The authors thank owners who consented to study of their dogs. The authors are grateful to Natasha Gauer and Elizabeth Baines for care of 4 of the clinical cases. N.H.B. gratefully acknowledges the Alice Noakes Trust for sponsoring his residency. P.J.W. s senior lectureship is funded by the Bunning endowment and Iams. This work carried out at Queen s Veterinary School Hospital, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge. This study was not supported by any grants. References 1. Miller ME, Evans HE. The digestive apparatus and the abdomen. In: Miller ME, Evans HE, eds. Miller s Anatomy of the Dog. Philadelphia, PA: WB Saunders; 1993: Guilford WG, Strombeck DR. Diseases of swallowing. In: Guilford WG, Center SA, Strombeck DR, Williams DA, Meyer DJ, eds. Strombeck s Small Animal Gastroenterology, 3rd ed. Philadelphia, PA: WB Saunders; 1996: Washabau RJ, Hall JA. Diagnosis and management of gastrointestinal motility disorders in dogs and cats. Comp Contin Educ Pract Vet 1997;19: Peeters ME, Ubbink GJ. Dysphagia-associated muscular dystrophy: A familiar trait in the Bouvier des Flandres. Vet Rec 1994;134: Stickle R, Sparschu G, Love N, Walshaw R. Radiographic evaluation of esophageal function in Chinese Shar Pei pups. J Am Vet Med Assoc 1992;201: Watrous BJ. Clinical presentation and diagnosis of dysphagia. Vet Clin North Am Small Anim Pract 1983;13: Heuschkel RB, Fletcher K, Hill A, et al. Isolated neonatal swallowing dysfunction: A case series and review of the literature. Dig Dis Sci 2003;48: Diamant N, Szczepanski M, Mui H. Idiopathic megaesophagus in the dog: Reasons for spontaneous improvement and a possible method of medical therapy. Can Vet J 1974;15: Rosario JA, Medow MS, Halata MS, et al. Nonspecific esophageal motility disorders in children without gastroesophageal reflux. J Pediatr Gastroenterol Nutr 1999;28: Schwartz A, Ravin CE, Greenspan RH, et al. Congenital neuromuscular esophageal disease in a litter of Newfoundland puppies. J Am Vet Radiol Soc 1976;17: Kipnis RM. Megaoesophagus: Remission in 2 dogs. J Am Anim Hosp Assoc 1978;14: Kahrilas PJ, Dodds WJ, Hogan WJ. Effect of peristaltic dysfunction on esophageal volume clearance. Gastroenterology 1988;94: Henderson RD, Mugashe F, Jeejeebhoy KN, et al. The role of bile and acid in the production of esophagitis and the motor defect of esophagitis. Ann Thorac Surg 1972;14: Lundell L, Myers JC, Jamieson GG. Is motility impaired in the entire upper gastrointestinal tract in patients with gastroesophageal reflux disease? Scand J Gastroenterol 1996;31: Watrous B, Suter PF. Normal swallowing in the dog. Vet Radiol 1979;20: Houlton JEF, Herrtage ME, Taylor PM, Watkins SB. Thoracic esophageal foreign bodies in the dog: A review of ninety cases. J Small Anim Pract 1985;26: Moore AH. Removal of esophageal foreign bodies in dogs: Use of the fluoroscopic method and outcome. J Small Anim Pract 2001;42: