Distal esophageal sphincter achalasia in a Labrador retriever dog with polypoid gastric mucosal hyperplasia and pyloric stenosis

Abstract

An 11-year-old, neutered female, Labrador retriever dog was presented with a history of intractable vomiting, regurgitation, and coughing. Computed tomography (CT) imaging identified marked hypertrophy of the distal esophagus with a suspicion of distal esophageal achalasia, based on the observation of a “bird beak” appearance. This was later confirmed on a fluoroscopic swallow study. Marked hypertrophy of the gastric pylorus was also identified on CT imaging, and polypoid gastric mucosal hyperplasia was diagnosed based on the gross endoscopic appearance combined with gastric histopathology. Secondary aspiration pneumonia was diagnosed based on the results of CT imaging, bronchoscopy and bronchoalveolar lavage fluid analysis. Medical therapy alone failed to elicit any significant improvement, but clinical resolution was achieved following surgical intervention comprising Ventral Heller myotomy, Dor’s fundoplication, and pyloroplasty.

Case description

An 11-year-old, neutered female, 36-kg, Labrador retriever dog was referred for further investigation of intractable vomiting, regurgitation, and coughing which had been progressive over the previous 3 wk. The initial clinical sign had been intermittent vomiting of undigested food several hours after feeding, with the later development of frequent regurgitation of white froth and food remnants. At the time of referral, the dog was unable to keep down either food or water and, despite a ravenous appetite, had lost 6 kg in body weight (BW). A right lateral thoracic radiograph taken 10 d before referral had shown only a moderate diffuse bronchointerstitial lung pattern, and a right lateral abdominal radiograph had been unremarkable. No orthogonal views had been taken. Previous treatment with maropitant (Cerenia; Zoetis UK, London, UK), 2 mg/kg BW, PO, q24h, ranitidine (Zantac; Sanofi UK, Guildford, Surrey), 3 mg/kg BW, PO, q8h, amoxicillin-clavulanate (Noroclav; Norbrook Laboratories UK, Corby, Northamptonshire, UK), 15 mg/kg BW, PO, q12h, prednisolone (Prednidale; Dechra, Stoke on Trent, Staffordshire, UK), 0.5 mg/kg BW, PO, q12h, propentoxyphylline (Vivitonin; Intervet UK, Walton, Milton Keynes, UK), 3 mg/kg BW, PO, q12h, and furosemide (Millpledge Veterinary, Retford, Nottinghamshire, UK), 0.5 mg/kg BW, PO, q12h, prescribed by the referring veterinarian, were reported to have resulted in no clinical improvement.

On physical examination the dog was depressed and approximately 7% dehydrated. Body condition score remained slightly excessive (6/9) but there was marked muscle atrophy. The respiratory rate was normal but there was excessive panting and a marked increase in respiratory effort. Thoracic auscultation revealed harsh lung sounds bilaterally, and gurgling was noted on auscultation over the thoracic inlet. Abdominal palpation was mildly resented and induced an episode of vomiting. Apart from stiffness in multiple limb joints, consistent with a previous diagnosis of degenerative joint disease, the remainder of the routine clinical examination, including neurological examination and rectal temperature, was unremarkable. The SpO₂ on room air was 96%, increasing to 99% with oxygen supplementation. Average systolic blood pressure was 100 mmHg.

Serum biochemistry identified azotemia which resolved following IV fluid therapy [creatinine: 152 μmol/L, reference range (RR): 0 to 125 μmol/L; urea: 25 mmol/L, RR: 1.7 to 9.0 mmol/L]. Mild alkaline phosphatase elevation (210 U/L, RR: 0 to 90 U/L) and mild hypoproteinemia (total protein: 43.9 g/L, RR: 53 to 78 g/L) were also present. A complete blood (cell) count (CBC) identified moderate mature neutrophilia (24.6 × 10⁹/L, RR: 2.9 to 11.6 × 10⁹/L). Urinalysis and fecal analysis were unremarkable. Further serological tests were submitted several days later to eliminate systemic causes of esophageal dysmotility. A negative acetyl choline receptor antibody titer ruled out myasthenia gravis, normal total thyroxine (T4), and thyroid-stimulating hormone (TSH) concentrations ruled out hypothyroidism, and normal resting cortisol concentrations made hypoadrenocortism unlikely.

On admission to the hospital the dog received IV fluid therapy (Hartman’s solution 4 mL/kg BW per hour) and oxygen supplementation. Single injections of maropitant (Cerenia), 1 mg/kg BW, IV, and omeprazole (Sandoz, Camberley, Surrey, UK), 1 mg/kg BW, IV were administered. The following day, intermittent regurgitation and a moderate increase in respiratory effort were ongoing, but the dog was assessed to be stable enough (normal hydration status, systolic blood pressure: 125 mmHg, respiratory rate: 24 breaths/min, SpO₂ 99% on oxygen) to proceed with further investigations which comprised thoracic computed tomography (CT) imaging, gastrointestinal endoscopy, and bronchoscopy. Following pre-oxygenation, and premedication with butorphanol (Dolorex; MSD Animal Health, Milton Keynes, Buckinghamshire, UK), 2 mg/kg BW, IV, and ketamine (Narketan; Vétoquinol UK, Buckingham, UK), 5 mg/kg BW, IV, general anesthesia was induced with propofol (Propoflo; Zoetis UK, Alton Oaks, Surrey, UK), 2 mg/kg BW, IV, and maintained with inhaled isoflurane (IsoFlo; Zoetis UK, London, UK). An arterial catheter was placed to facilitate ongoing monitoring of oxygenation status.

Computed tomography imaging showed marked (up to 15 mm), circumferential, symmetrical thickening of the distal esophageal wall, spanning the distal esophageal sphincter into the proximal cardia. This was causing marked narrowing of the caudal 3.5 cm of the esophageal lumen and, on the sagittal MPR view, was noted to have a “bird beak” morphology consistent with achalasia (1–3) (Figure 1). Similar moderate (up to 8 mm), circumferential, symmetrical thickening was evident in the region of the gastric pylorus, pyloric sphincter, and proximal duodenum, resulting in a reduced diameter of the pyloric outflow tract. Normal wall-layering and contrast enhancement was preserved in all affected areas making concentric hypertrophy the most likely explanation. Fluid was present within the most dependent aspect of the caudal cervical trachea and a diffuse increase in peri-bronchial attenuation was evident throughout the lung fields, along with marked ventral consolidation. The right cranial, middle, and caudal lung lobes were particularly affected, with focal areas of consolidation also present in the accessory lung lobe. These findings were consistent with aspiration pneumonia and underlying chronic bronchitis.

Figure 1.

Sagittal, multiplanar reconstructed (MPR), enhanced soft tissue window, thoracic CT image (cranial aspect on the left) showing marked circumferential, symmetrical thickening of the distal esophageal wall. Note the obstruction of the distal 3.5 cm of the distal esophageal lumen (black asterisk) with associated “bird beak” morphology (red arrows) and moderate gassy esophageal dilation proximally (white asterisk).

On gastrointestinal endoscopy the esophageal mucosa was unremarkable, but the distal esophageal sphincter had a hypertrophied appearance which was obscuring the cardia (Figure 2). Distal esophageal sphincter tone was assessed to be increased, making it difficult to pass even a small endoscope into the cardia (Multi-purpose video-endoscope 60714PKS/NKS, 7.9 mm sheath; Karl Stortz, Dundee, UK). The gastric fundus was unremarkable, but the pyloric antrum was grossly abnormal containing many variably sized, prominent, mildly hyperemic polypoid and sessile lesions (Figures 3a and 3b). The pyloric sphincter, similar to the distal esophageal sphincter, also had a hypertrophied appearance (Figures 3a and 3b) and an apparent increase in tone, making it difficult to pass the endoscope into the duodenum. The duodenal mucosa was grossly unremarkable. Endoscopic biopsies obtained from the distal esophagus, stomach, and duodenum were submitted for histopathology. This showed mild multifocal neutrophilic esophagitis, mild multifocal lymphocytic, plasmacytic, and eosinophilic gastritis, and mild diffuse chronic lymphocytic and plasmacytic enteritis with multifocal eosinophilic infiltrates.

Figure 2.

Endoscopic view of distal esophagus showing hypertrophy of the cardiac sphincter.

Figure 3.

Endoscopic views (a) and (b) of the pyloric antrum showing multiple, variably sized, prominent, polypoid and sessile lesions, and pyloric hypertrophy.

Bronchoscopy (Video-bronchoscope 11900BN; Karl Stortz) identified mild, diffuse hyperemia and rounding of the lower airways with multi-focal dynamic airway collapse. In several locations, turbid watery fluid and pale solid fragmented material (presumed to be ingesta) were noted within the airway lumens. Similar particulate fluid was also suctioned from the trachea and endotracheal tube throughout the procedure. Cytology of bronchoalveolar lavage (BAL) fluid identified moderate to marked neutrophilic inflammation with moderate numbers of small, plump free and intracellular bacilli, and clumps of basophilic material presumed to be ingesta. Culture of the BAL yielded a moderate growth of a multi-drug resistant Escherichia coli.

Following recovery from anesthesia, treatment with oxygen supplementation, IV fluid therapy (Hartman’s solution + 20 mmol/L KCl), 4 mL/kg BW per hour, metoclopramide (Vomend, Dechra Pharmaceuticals), 1 mg/kg BW per day constant rate infusion (CRI), maropitant (Cerenia), 1 mg/kg BW, IV, q24h, omeprazole (Sandoz), 1 mg/kg BW, IV, q12h, ranitidine (Alliance Pharmaceuticals, Chippenham, Wiltshire, UK), 3 mg/kg BW, IV, q8h, and empirical broad-spectrum antibiotic therapy [amoxicillin-clavulanate (Augmentin; Beecham Group, Uxbridge, Middlesex, UK), 20 mg/kg BW, IV, q8h, and metronidazole (AAH Pharmaceuticals, Talke, Stoke-on-Trent, UK), 10 mg/kg BW, IV, q12h], was continued. Treatment with amoxicillin-clavulanate and metronidazole was discontinued and replaced with marbofloxacin (Marbocyl; Vétoquinol), 2 mg/kg BW, IV, q24h, 2 d later when the results of BAL culture and antibiotic susceptibility testing identified an E. coli infection with in vitro resistance to amoxicillin, amoxicillin-clavulanate, cephalexin, tetracycline, and clindamycin. In vitro sensitivity to marbofloxacin and enrofloxacin was documented and it was later confirmed that the isolate was not an extended spectrum beta-lactamase (ESBL)-producing strain.

Three days later, frequent regurgitation continued despite elevated feeding with food of a variety of consistencies. A fluoroscopic swallow study (using barium mixed with food) demonstrated a normal pharyngeal phase of swallowing, followed by a markedly abnormal distal esophageal phase. The latter was characterized by delayed transit time, accumulation of ingesta in the thoracic esophagus, and subsequent distal esophageal dilation (Figure 4). The distal esophageal wall was thickened resulting in marked narrowing of the lumen. As noted on CT imaging, this produced a “bird beak” sign (Figure 4), consistent with esophageal achalasia (1–3). Passage of barium into the stomach was delayed and was accompanied by gastroesophageal reflux. Since the dog was persistently vomiting and regurgitating, it was not possible to perform pyloroduodenal transit studies, thus pyloric sphincter function could not be fully evaluated.

Figure 4.

Lateral fluoroscopic image of the esophagus during the video-fluoroscopy swallow study (cranial aspect on the left). Note the marked dilation of the distal thoracic esophagus with ingesta, and the conical tapering of the distal aspect of the esophagus forming a narrow “bird beak” sign (black arrows).

Persistent vomiting and regurgitation meant that it was impossible to prevent ongoing aspiration, or to supply adequate enteral nutrition. At this time, it was deemed unlikely that any further progress would be made with medical therapy and the decision was made to proceed with surgical intervention. Following pre-oxygenation, the dog was premedicated with methadone (Comfortan; Dechra Pharmaceuticals, Norwich, UK), 0.2 mg/kg BW, IV, and ketamine (Narketan; Vétoquinol UK), 2 mg/kg BW, IV. Anesthesia was induced with propofol (Propoflo; Zoetis UK, Alton Oaks, Surrey, UK), 2 mg/kg BW, IV, and maintained with isoflurane (IsoFlo; Zoetis UK, London, UK). Alfentanil (Rapifen; Janssen Cilag, High Wycombe, Buckinghamshire, UK), 3 μg/kg BW, IV bolus followed by 0.5 mg/kg BW per minute CRI was given for analgesia. The dog was prepared for exploratory laparotomy, a xypho-umbilical incision was made, and a Heller’s esophagomyotomy was performed as previously described (4,5). The lateral attachment of the left liver lobe was released, and the cardia and distal esophagus were dissected free from the phrenic ligament while protecting the ventral vagus nerve. The distal 4 cm of the esophagus was isolated, and a ventral adventitia-muscular incision was made from the distal 3 cm of the esophagus, the cardia, and the proximal 3 cm of the stomach. The adventitia and muscle were then separated from the mucosa with hemostatic forceps. A large oro-gastric tube was placed to help with dissection and the stomach was insufflated to confirm the absence of mucosal perforation (Figure 5). To prevent gastro-esophageal reflux, a Dor’s fundoplication was performed as previously described (4). The gastric fundus was pulled ventrally from the left side and sutured first to the lateral aspect of the esophagomyotomy incision (Figure 6a), and then to the right side, to achieve full coverage of the mucosal defect. In order to enhance the stability of the cardia and prevent intra-thoracic displacement, the most cranial sutures on the left and right sides of the fundoplication incorporated the edge of the esophageal hiatus and gastric fundus, creating an esophagopexy (Figure 6b). A large gastrostomy tube (Mic, 14 Fr, Halyard) was placed in the left gastric antrum (6) to permit postoperative decompression of the stomach and to facilitate early enteral feeding. To relieve the suspected pyloric obstruction, a Y-U antral pyloroplasty was performed as previously described (6). A biopsy was obtained from the gastric wall and the largest of the polypoid antral lesions (12 × 9 × 7 mm) was resected. Histopathology of the polyp subsequently showed papillomatous expansion of the gastric mucosa, mild lymphoplasmacytic infiltration adjacent to the blood vessels, and slightly irregular smooth muscle myofiber bundles. This benign proliferative morphology is consistent with polypoid mucosal hyperplasia. After surgery, medical treatment was continued as previously, with the addition of multimodal analgesia including lidocaine (Hamlen Pharmaceuticals, Gloucester, UK), 2 mg/kg BW per hour CRI, ketamine (Narketan), 10 μg/kg BW per hour CRI, and methadone (Comfortan; Dechra Pharmaceuticals), 0.2 mg/kg BW, IV, q4h. Monitoring of blood pressure and PaO₂ was continued, and hourly gastric decompression was performed to monitor for postoperative ileus. Gastrotomy tube feeding was initiated 24 h after surgery (Formula V Enteral Care KC Canine; PetAg, Hampshire, Illinois, USA). One-third of the resting energy requirement (RER) was supplied initially, increasing to two-thirds RER after 2 d and to the full RER on day 5. Serum proteins, electrolytes, and PCV were monitored daily, and a CBC and serum biochemistry were repeated on day 3. Except for mild hypokalemia, which resolved following additional intravenous supplementation, these results raised no additional concerns.

Figure 5.

Intraoperative view of the Heller’s esophagomyotomy, ventral laparotomy (cranial aspect on the left). A complete esophagomyotomy has been performed extending for 3 cm over the distal esophagus (arrow), cardia (*), and cranial stomach. A probe is pushing the left edge of the myotomy wound laterally, and additional stay sutures are present on each side of the wound facilitating caudo-ventral retraction. Note the clear bulging of the esophago-gastric mucosa through the sero-muscular wound.

Figure 6.

a — Intraoperative view of the Dor’s fundoplication stage 1, ventral laparotomy (cranial aspect on the left). The dorsal gastric fundus cranial to the splenogastric ligament has been pulled ventrally to be sutured to the edges of the esophagomyotomy with minimum tension. The most medial part is first sutured to the lateral part of the myotomy along the length of the defect, on the left side (arrowheads). At this stage the esophageal mucosa is still not covered by serosa and is seen bulging through the edges of the wound (*). The right side of the esophagomyotomy wound is still left uncovered (long dashed arrows). b — Intraoperative view of the Dor’s fundoplication stage 2, ventral laparotomy (cranial aspect on the left). The right edge of the myotomy is now sutured to the most dorsal part of the gastric fundus (dashed arrows). The increased rotation of the fundus around the myotomy is proven by the observation of the gastro-splenic ligament and spleen ventrally (small arrows). The most proximal sutures include the right diaphragmatic crus to increase stability of the caudal esophagus within the abdomen. At this stage the mucosa is fully covered by the sero-muscular wrap ventrally (180 degrees fundoplication).

For the first 48 h after surgery the dog remained depressed with a moderate increase in respiratory effort, but tube feeding was well-tolerated with no episodes of vomiting or regurgitation. Over the subsequent few days there was gradual improvement and, by the time of discharge 1 wk after surgery, the dog was bright and eating normally with only a mild increase in respiratory effort. Oral therapy with omeprazole (TEVA UK, Eastbourne, UK), 40 mg PO, q12h, and marbofloxacin (Marbocyl; Veterinary Medical UK), 80 mg PO, q24h, was continued and tramadol (Almus Pharmaceuticals, Actavis, Barnstaple, UK), 75 mg PO, q8h, was introduced for management of arthritic pain which was perceived to have worsened as a result of prolonged confinement.

Two weeks following surgery the dog remained bright with a good appetite. She was consuming her full caloric requirement PO, with no further vomiting or regurgitation, so the gastrotomy tube was removed. Respiratory effort was normal and exercise tolerance was reported to be better than it had been before the onset of clinical signs. During endoscopic removal of the gastrotomy tube the previously encountered structural narrowing of the distal esophageal sphincter and pylorus was improved and passage of the endoscope through the distal esophageal and pyloric sphincters was now unimpaired. Repeat fluoroscopy demonstrated a marked improvement in esophageal transit, and the “bird beak” sign was no longer evident (Figure 7). Two years after surgery the dog remains asymptomatic. The final diagnosis was distal esophageal sphincter achalasia associated with polypoid gastric mucosal hyperplasia and pyloric stenosis.

Figure 7.

Lateral fluoroscopic image of the esophagus during the follow-up video-fluoroscopy swallow study 2 wk post-surgery (cranial aspect on the left). The image was obtained during the esophageal phase as the bolus progressed towards the stomach. The previous “bird beak” sign is no longer present and the esophagus is much less dilated.

Discussion

The term achalasia means failure of relaxation and is generally used with reference to visceral junctions. Achalasia results from localized degeneration and loss of ganglionic cells, predominantly of inhibitory neurons, leading to smooth muscle spasm and subsequent impairment to the passage of ingesta (1,2). Distal esophageal sphincter achalasia is the most commonly recognized motor disorder of the esophagus in humans, usually presenting as a combination of dysphagia, regurgitation, weight loss, chest pain, and aspiration pneumonia (1,2,7). There are few previous reports of distal esophageal sphincter achalasia in dogs (5,8–11). In these previous reports the dogs were presented with comparable clinical signs; however, unlike in humans, concurrent megaesophagus was a consistent feature. It is unclear whether this is a late-stage sequela, or whether it represents a distinct disease entity.

Although the etiology of distal esophageal sphincter achalasia remains uncertain, autoimmunity has been implicated and is supported by several studies (1,2,12). Current evidence suggests that an external influence (such as occult viral infection) incites inflammation of the myenteric plexus, triggering an autoimmune response in a susceptible population which may be genetically predisposed (1,2,12). Patients with idiopathic achalasia are more likely to suffer from a concurrent autoimmune condition compared with the general population, with several studies reporting significant associations with hypothyroidism, diabetes mellitus, systemic lupus erythematosus, and uveitis (1,12). Secondary achalasia refers to the development of achalasia because of an underlying disease. Reported causes include MEN2A syndromes, paraneoplastic syndromes, chronic intestinal obstruction, persistent gastrointestinal reflux, Chagas disease, and infiltrative esophageal pathology (e.g., amyloidosis, sarcoidosis, neurofibromatosis, eosinophilic esophagitis) (1–3). Identification of concurrent inciting pathology is of paramount importance because, while idiopathic achalasia can be effectively treated with Heller myotomy (4,13), the treatment of secondary achalasia must be directed at the underlying disease. Mucosal hypertrophy, muscularis thickening, and aberrant esophageal contractions must also be distinguished from obstructive conditions such as esophageal neoplasia, esophageal polyps, or hiatal hernia (3,14). Various diagnostic imaging modalities may be required to confirm the diagnosis, but the hallmark of esophageal achalasia is a gradual tapering and smooth conical narrowing (“bird’s beak” appearance) of the distal esophageal segment (1–3). Confirmation of elevated distal esophageal sphincter pressures via manometry is sometimes used to further support the diagnosis (1,2,7).

Gastric polyps are rarely recognized in dogs but, as in humans, they are usually asymptomatic and are generally an incidental post-mortem finding (15). An association with pyloric obstruction has been reported previously in dogs (16–18) and, although not present at the time of endoscopy, this may have provided a stimulus for the development of pyloric hypertrophy and stenosis in our patient. Alternatively, idiopathic pyloric achalasia may have been the initiating factor, culminating in chronic gastric inflammation with subsequent polyp formation. The concurrent existence of esophageal achalasia and pyloric pathology has not previously been reported in dogs but is described in humans (19–21).

Combined Heller’s esophagomyotomy and Dor’s fundoplication is the recommended surgical treatment for distal esophageal achalasia in humans (4,7,13). This is, to our knowledge, the first report of the combined procedure in a canine patient. Previous case reports have described esophagomyotomy alone, but this has been either unsuccessful in relieving the clinical signs or with limited follow-up (5,8–11). Dor’s fundoplication is performed following esophageal myotomy as an anti-reflux procedure. This has been shown to be the most successful fundoplication method in human patients (22). A Dor’s plicature is performed on the ventral (anterior) surface of the esophagus and involves bringing only the ventral half (180 to 200 degrees) of the gastric cardia onto the esophagus. This appears less likely to generate an area of focal constriction which could potentially aggravate the pre-existing dysphagia, as has been observed with Nissen fundoplication which uses a 360-degree wrap (4,22). In our patient, no regurgitation has been observed since the time of surgery. Pyloroplasty and excision of the largest gastric polyp appeared to effectively relieve the pyloric obstruction in this dog. Y-U pyloroplasty has been reported as a simple and efficient procedure to relieve pyloric obstruction and is less invasive and safer than pylorectomy and Billroth I anastomosis (6).

The signalment, clinical signs, fluoroscopic evaluation, and complete response to a Ventral Heller myotomy, fundoplasty, and pyloroplasty, provide evidence that the dog in this report had acquired distal esophageal achalasia, pyloric stenosis, and polypoid gastric mucosal hypertrophy. To the authors’ knowledge, this condition and combination of procedures has not been previously described in dogs.

In summary, distal esophageal achalasia should be part of the differential diagnosis for dogs with persistent regurgitation and diagnosis requires a fluoroscopic contrast esophagram using food mixed with barium. Polypoid gastric mucosal hypertrophy should be considered as an uncommon cause of persistent vomiting. Finally, the complete response to Ventral Heller myotomy, fundoplasty, and pyloroplasty, with a 2-year follow-up period, provides support for the use of this surgical procedure in future patients. CVJ