Veterinary Endoscopy
0195-5616/90 $0.00
+ .20
Upper Gastrointestinal Endoscopy W. Grant Guilford, BVSc, BPhil*
Upper gastrointestinal (GI) endoscopy is the most frequently performed GI endoscopic procedure at the University of California, Davis, Veterinary Medical Teaching Hospital (Fig. 1). Upper GI endoscopy is a relatively noninvasive, atraumatic technique that permits visual examination of esophageal, gastric, and upper small bowel lesions and allows descriptive or photographic documentation of their severity and extent. Endoscopy provides biopsy, cytology, and fluid samples for laboratory evaluation. It allows therapeutic interventions such as foreign body retrieval, bougienage, and gastrostomy tube placement. It has a low morbidity and mortality but should only be used after routine work-up has failed to reveal a diagnosis.
INDICATIONS AND LIMITATIONS Upper GI endoscopy is most useful for the diagnosis of esophageal, gastric, and upper small intestinal disorders with a mucosal or luminal location. Lesions located in the muscular and submucosal layers of the bowel are more difficult to detect with an endoscope. Endoscopy and endoscopic biopsy ~etects morphologic but not functional disease. It will not detect abnormal GI motility, GI hypersecretory disorders, and subcellular defects such as brush border enzyme deficiencies. Because of restricted working length, current endoscopes cannot be used to evaluate mid-small intestinal disease. The clinical problems commonly evaluated by upper GI endoscopy are listed in Table 1. Upper Gastrointestinal Endoscopy Versus Contrast Radiography Upper GI contrast radiography and endoscopy are complementary procedures. Endoscopy is more sensitive for the diagnosis of mucosal diseases of the upper GI tract, and offers the important advantage of *Diplomate, American College of Veterinary Internal Medicine; Member, Small Animal Medicine Service, Veterinary Medical Teaching Hospital, and Research Fellow, Department of Physiological Sciences, University of California School of Veterinary Medicine, Davis, California Veterinary Clinics of North Am£rica: Small Animal Practice-Vol. 20, No. 5, September 1990
1209
1210
W.
Rhinoscopy
Bronchoscopy
24%
22%
GRANT GUILFORD
Figure l. Relative frequency of the different endoscopic procedures performed on 948 cats and dogs at University of California, Davis, Veterinary Medical Teaching Hospital. The miscellaneous category includes laryngoscopy, vaginoscopy, urethroscopy, laparoscopy, and thoracoscopy procedures. (From Strombeck DR, Guilford WG: Small Animal Gastroenterology, ed 2. Davis, CA, Stonegate Publishing, 1990; with permission.)
definitive diagnosis through tissue collection (cytology and biopsy). Contrast procedures do not require anesthesia, and they provide a better estimation of luminal diameter (esophagus), mural masses, extramural compressive lesions, jejunal diseases, GI motility, and gastric emptying. The prime function of the esophagus is one of motility. Disordered motility from esophageal neuromuscular disease is the most common cause Table 1. Principal Indications for Upper Gastrointestinal Endoscopy Evaluation of dysphagia Evaluation of regurgitation Evaluation of chronic vomiting Evaluation of hematemesis Evaluation of melena Evaluation of chronic diarrhea Retrieval of esophageal foreign bodies Bougienage of esophageal strictures Retrieval of select gastric foreign bodies Placement of percutaneous gastrostomy tubes
UPPER GASTROINTESTINAL ENDOSCOPY
1211
of esophageal dysfunction. Therefore, in most cases of suspected esophageal disease, barium swallows, preferably with fluoroscopy, are performed before endoscopy. The principal functions of the stomach and intestine are motility, secretion, and assimilation. Most disease processes that perturb these functions have a morphologic basis. Radiography is less sensitive than endoscopy for the detection of morphologic disease of the stomach in the dog. 6 Furthermore, radiography can localize morphologic disease, but can rarely define its cause. Therefore, in most cases of suspected gastroduodenal disease, endoscopic examination should precede contrast radiographic procedures. When endoscopy was used prior to contrast radiography for the diagnosis of suspected upper GI disease in a series of human patients, only 5% of the persons subsequently required barium studies. In comparison, when contrast radiography was the first procedure, 30% of the patients subsequently required endoscopy. 9 Combination Upper and Lower Gastrointestinal Endoscopy
It is the preference of some veterinary gastroenterologists to perform both gastroduodenoscopy and colonoscopy regardless of the character of the presenting signs. The endoscopic examination of the entire GI tract in one session has the advantage that subclinical disease in another part of the intestinal tract may be detected. This is particularly true of the inflammatory bowel diseases, disorders that do not respect the pylorus or ileocolic junction as an inviolate boundary. It is the preference of this author, however, to reserve the "hi-orifice" approach for patients that manifest signs of GI disease clearly referable to both large and small bowel dysfunction. The rational for this "uni-orifice" approach is that subclinical disease in another part of the GI tract only occasionally affects subsequent therapeutic approach or treatment success. In the opinion of this author, the extra expense and time involved in the "hi-orifice" approach is therefore rarely warranted. CONTRAINDICATIONS There are few absolute contraindications to performing GI endoscopy. The most common contraindication is patients that have an increased anesthetic risk. The procedure is not appropriate if bowel perforation is suspected, because contamination of the surrounding tissues may be increased as a result of the pressurization of the GI tract by air insuffiation. Endoscopy is discouraged in patients with inadequately prepared GI tracts, and in animals with bleeding diatheses.
COMPLICATIONS Complications of upper GI endoscopy are rare. Those most frequently encountered are listed in Table 2. Perforation of the esophagus with resultant mediastinitis and pleuritis or of the stomach or intestine with
1212
W.
GRANT GUILFORD
Table 2. Most Common Complications of Gastrointestinal Endoscopy GI perforation Laceration of major blood vessels Laceration of organs adjacent to the GI tract Decreased venous return owing to gastric overdistension Acute bradycardia Gastric·dilatation volvulus Mucosal hemorrhage Transmission of enteropathogenic organisms Bacteremias* *Incidence uncertain in veterinary medicine.
consequent peritonitis can result from forceful insertion of the endoscope, especially in the absence of vision of the lumen. Most commonly, however, perforation results from poor biopsy or retrieval technique. If a perforation is suspected, immediate radiography will usually confirm the diagnosis as large quantities of air rapidly escape the viscus to enter the surrounding body cavity. It can be difficult to detect the presence of small perforations by endoscopy. Gastric-dilatation-volvulus can occur following endoscopic procedures, perhaps owing to inadequate removal of insufflated air. Overdistension of the stomach with air during the procedure results in compression of the caudal vena cava and a rapid drop in venous return and blood pressure. Unless rapidly recognized and corrected, this is quickly fatal. Acute bradycardia, apparently due to vagovagal reflexes, can occur during endoscopy. This phenomenon most often occurs when the instrument enters the small intestine of small breeds and is perhaps caused by overdistension of the intestinal tract or by excessive traction on the mesentery. Major blood vessels can be ruptured during removal of foreign bodies and during bougienage. Rarely, considerable hemorrhage can follow biopsy procedures. Poorly disinfected scopes can transmit enteropathogenic organisms. Following routine endoscopy, oropharyngeal organisms can be transiently cultured from the blood of a small percentage of human patients. Whether the same phenomenon occurs in the· dog and cat is unknown.
PATIENT PREPARATION During the 12 to 24 hours prior to the endoscopic procedure, food should be withheld from the patient, and symptomatic therapy should be instituted to address any fluid or electrolyte abnormalities that may compromise anesthetic safety. Food should be withheld for a longer period if there is evidence of delayed gastric emptying. Retained gastric material interferes with visualization, may obstruct the operating/suction channel of the endoscope, and may result in pulmonary aspiration during anesthesia recovery. Anesthesia Anesthesia is essential for upper GI endoscopy. The anesthetic regimen chosen is de pendent on the animal's general condition and the presence of
UPPER GASTROINTESTINAL ENDOSCOPY
1213
any intercurrent disease. As a rule, inhalation anesthesia is used most frequently because of its safety and ease of administration. Anticholinergic premedication is an advantage to reduce gastric motility and secretion. Unfortunately, pyloric tone is not reduced by anticholinergics. Narcotics agents increase pyloric and cranial duodenal tone in humans, interfering with the easy passage of the scope. 5 The author's clinical impression is that a similar phenomenon occurs in dogs. Therefore, if the condition of the animal allows, thes€ drugs are best avoided during GI endoscopy. The anesthetist must be particularly alert for the signs of gastric overinflation, which include excessive abdominal distension, tachycardia, pale mucous membranes, and a precipitous drop in blood pressure, and for acute onset of bradycardia suggestive of vagovagal reflexes. Patient Positioning For routine upper GI endoscopy the patient is positioned in left lateral recumbency. This allows gastric juices to gravitate to the left side, away from the pyloric antrum and pylorus, and facilitates insufflation of the antrum. For the placement of gastrostomy tubes, the patient should be placed in right lateral recumbency. A reliable gag must always be placed in the mouth to protect the endoscope.
ENDOSCOPIC EXAMINATION Description of the Mucosa Written description of the mucosa should become part of the record of any animal undergoing endoscopy. Where appropriate, photographic records can also be kept. Consistent description of mucosal lesions is assisted by the preparation of endoscopy grading sheets for inclusion in the record. Grading sheets should include a description of the size and position of any lesions such as masses or ulcers. In addition, each of the following parameters should be evaluated in a semiquantitative fashion: degree of mucosal erythema, friability, granularity, and erosions; the amount of mucus; and the visibility of submucosal blood vessels. Of these parameters, increased mucosal erythema is least likely to correlate closely to the presence of mucosal disease. The appearance of the mucosa varies considerably with degree of insufflation. Esophagoscopy Flexible endoscopes allow the most thorough examination of the esophagus but rigid endoscopes can be used and may have some advantages in the removal of sharp foreign bodies. The endoscope is directed through the upper esophageal sphincter and the esophagus insufflated with air until sufficiently distended to visualize the lumen. The tip of the endoscope is then slowly advanced to the gastroesophageal junction. There may be a redundancy of tissue at the thoracic inlet that gives the impression of a diverticulum, but that can usually be largely obliterated by full extension
1214
W.
GRANT GUILFORD
Figure 2. Normal gastroesophageal junction.
of the neck. Pulsations of the esophagus will be present as one passes the endoscope over the heart. The normal mucosa is pale and smooth. Submucosal vessels are usually not visible. The luminal diameter of the esophagus can be hard to judge by endoscopy. In the anesthetized animal the normal esophagus appears flaccid and may partially drape over thoracic vasculature. For these reasons, be wary of diagnosing megaesophagus based on endoscopic judgment only. The gastroesophageal junction has a slit-like appearance (Fig. 2). Slight
Figure 3. Gastroesophageal junction of a 2-year-old rottweiler with chronic and severe esophagitis. Note the prominent mucosal irregularity. (Courtesy of Dr. Kim Robertson, University of California, Davis, Veterinary Medical Teaching Hospital.)
UPPER GASTROINTESTINAL ENDOSCOPY
1215
reddening may be apparent at the gastroesophageal junction in normal animals. When present, esophagitis may or may not be visually apparent. If it is apparent, erythema, erosions, irregularity, and strictures may be seen (Fig. 3). Because of its durable epithelium and tubular shape, biopsy of the esophagus is more difficult than the biopsy of other parts of the GI tract. The Quinton (Quinton Instrument Co, Seattle, WA) suction biopsy instrument is the safest and most effective method to collect a biopsy from the esophagus. Gastroscopy Following examination of the esophagus, the endoscope is gently advanced through the gastroesophageal sphincter into the stomach. On entry into the stomach, the mucosa of the undistended stomach usually obstructs most of the field of vision until the stomach is sufficiently insuffiated. The first part of the stomach wall that is visualized is usually the junction of the fundus and body. The lesser curvature is characterized by fewer, straighter mucosal folds than the greater curvature. Slight deviation of the tip of the scope away from the mucosa will allow the endoscopist to obtain a panoramic view of the body of the stomach as it is inflating. The endoscopist should be cognizant of the readiness with which the stomach inflates and the rugal folds disappear. If the stomach does not inflate, consider the possibility that air is exiting the stomach via the esophagus (firmly occlude by digital pressure if necessary), that your equipment is not insufflating correctly, or that the stomach is unable to distend owing to extramural compression or an intramural lesion. Prominent rugal folds are usually due to ineffective insuffiation but hypertrophic gastropathy must be considered. Overdistension of the stomach should be avoided because it can impede venous return, decrease tidal volume, allow a "belly" to develop in the insertion tube that inhibits maneuverability of the endoscope, and increase antral and pyloric contraction frequency by way of the antral reflex, both of which make passage of the endoscope into the duodenum more difficult (Fig. 4). The large size of the stomach means that the endoscopist must develop a systematic approach to gastroscopy, otherwise lesions will be missed. Particular care should be taken to observe the fundus, cardia, and lesser curvature, all areas of the stomach easily overlooked if the tip of the endoscope is single-mindedly passed to the pylorus along the greater curvature. If fluid is retained in the stomach it usually pools in the fundus and greater curvature of the body. Pooled fluid assists identification of this area but inhibits visualization of the mucosa. Large volumes of retained fluid should be aspirated to facilitate mucosal examination and to prevent aspiration during recovery. The incisura angularis is an important landmark (Fig. 5). It is a narrow shelf of tissue that divides the pyloric antrum from the lesser curvature of the gastric body. Because the natural progression of an aborally directed endoscope is along the greater curvature of the stomach, it is often necessary to retroflex the tip of the endoscope firmly by up to 180 degrees away from
w.
1216
GRANT GUILFORD
Decreased tidal volume Lungs Initiation of the antral reflex Increased antral and pyloric contractility
Inability to pass endoscope into pylorus Endoscope "belly"
I Figure 4. Consequences of gastric overdistention. Gastric overdistention results in a "belly" in the insertion tube of the endoscope, which inhibits maneuverability, increases antral contractions and pyloric tone, and compromises venous return and tidal volume. (From Strombeck DR, Guilford WG: Small Animal Gastroenterology, ed 2. Davis, CA, Stonegate Publishing, 1990; with permission.)
the greater curvature to obtain an en face view of the incisura. Once the incisura is identified, the pyloric antrum will be seen on one side and the lesser curvature, with the cardia dimly identifiable in the distance, will be seen on the other side. The cardia is easily identified by the presence of the insertion tube of the endoscope (Fig. 6). Once in the antrum, the tip of the endoscope is slowly advanced toward the pylorus. Movement of the scope into and along the antrum is inhibited if the stomach is overdistended. During this part of the examination, be sure that the lesser curvature of the pylorus is examined closely because lesibns can be easily missed in this area, especially when using scopes with narrow angles of view. The normal pylorus will usually yield to gentle pressure and allow entry of the tip of the endoscope into the duodenum. If not, the normal pylorus may be relaxed with glucagon (0.05 mg/kg, not to exceed 1 mg, IV). In some animals glucagon will induce a pronounced tachycardia. Adroit manipulation of the endoscope is often necessary to penetrate the pylorus. The normal stomach mucosa is bright pink to red and is lighter in color in the pyloric region. There should be no evidence of erosions or
UPPER GASTROINTESTINAL ENDOSCOPY
1217
Figure 5. Close-up of the incisura angularis of the stomach. The incisura is an important landmark: It divides the lesser curvature and cardia (top left) from the pyloric antrum (bottom right).
friability, suggestive of gastritis, or any indication of submucosal vessels (with the exception of the cardia or overdistended stomachs). The observation of submucosal vessels suggests a diagnosis of atrophic gastritis. Broad areas of induration in association with mucosal erosion or ulceration are usually a result of gastric cancer (Color Plate A). In hypertrophic gastropathy, the rugae often appear thickened and strongly light reflective, suggestive of edema. Furthermore, the rugal hypertrophy may be focal, and the folds may extend into the antrum, where
Figure 6. Gastric cardia. The cardia is easily identified by the presence of the insertion tube of the endoscope.
1218
W. GRANT GUILFORD
Figure 7. Normal pylorus. The incisura angularis of the stomach is visible at the top right of the figure. Foam adheres about the pyloric antrum.
it is unusual in normal animals to find many rugae. Mucosal erosions or ulcers may be apparent. The pylorus of normal dogs has a wide variety of appearances (Fig. 7). In general it should have clean margins, should not be obscured by excessive folds, and usually demonstrates rhythmical opening and closing. Occasionally, gastroduodenal reflux will be noticed. This is a normal occurrence in many dogs and cats. A patient with a hypertrophic pylorus will have a history compatible with delayed gastric emptying, may have retained gastric ingesta, evidence of rugal hypertrophy and mucosal erosions (hypergastrinemia owing to chronic distension), and usually has an enlarged, muscularlooking, protuberant pylorus with a small pyloric canal that is unable to accommodate the scope (Fig. 8). Some common problems encountered by inexperienced endoscopists during gastric examination and some suggested remedies are listed in Table 3. Duodenoscopy
After passage through the pylorus, the endoscope enters the short cranial duodenum and immediately encounters the cranial duodenal flexure . This is a very acute flexure that can be difficult to negotiate. It arises because of the rapid change of the cranial-and-to-the-right angulation of the pylorus and cranial duodenum to the caudal orientation of the descending duodenum. To negotiate this flexure . it is often necessary to flex the endoscope tip maximally, torque the insertion tube, and use a slide-by technique. Torquing the instrument at this point will be difficult if there is excess "belly" in the insertion tube as it rounds the greater curvature. The normal duodenal mucosa has a velvety appearance and a slightly more granular and friable nature than the stomach. Submucosal vessels are
UPPER GASTROINTESTINAL ENDOSCOPY
1219
Figure 8. Pyloric hypertrophy. Note the protuberant and muscular appearance of this hypertrophic pylorus. (Courtesy of Dr. Brent Jones, University of Missouri.)
not usually apparent. Careful examination may reveal the duodenal papillae. Abnormal duodenal mucosa commonly develops a pronounced granularity and friability. Occasionally, circular patches of lipid-laden villi may be observed, which are characteristic of lymphangiectasia (Color Plate B). Completion of the Endoscopic Examination After the endoscope reaches its full working length, it is slowly retracted. Biopsies, brush cytology, and aspiration of fluid are undertaken as indicated. All air should be aspirated from the GI lumen before the endoscope is withdrawn. The animal should then be allowed to recover from anesthesia and closely observed for the complications discussed previously. ANCILLARY ENDOSCOPIC TECHNIQUES Brush Cytology Brush cytology is a useful adjunct to endoscopic biopsy. It should be performed prior to biopsy so that the cytologic specimen is not contaminated with blood from the biopsy site. It may improve diagnostic yield because
1220
W.
GRANT GUILFORD
Table 3. The Gastric Examination: Trouble Shooting Problem: Inability to visualize the gastric lumen Reason: Inadequate insuffiation. Can be due to rapid loss of air through the esophagus or pylorus; equipment failure, depression of aspiration button on the handpiece instead of or along with the insuffiation button; extragastric compression; gastric mural disease Remedy: Manually occlude the esophagus, check equipment function, continually depress insuffiation button to keep pace with rapid ongoing losses Problem: Pyloric antrum and pylorus in view but scope will not advance into the antrum or repeatedly "flips" over the angularis toward the cardia Reason: Gastric overdistension creating a belly in the endoscope Remedy: Withdraw scope to cardia, partially deflate stomach and try again Problem: Unable to negotiate pylorus Reasons: Increased pyloric tone owing to gastric overdistension, narcotic administration, etc.; lateral placement of the pylorus in the antrum; anatomic pyloric obstruction Remedy: Partially deflate stomach; torque endoscope to allow utilization of the maximum deflection capability; administer glucagon to reduce pyloric tone
superficial material that otherwise may be lost during processing is sampled. Thus, organisms such as protozoa that reside in the mucus of the gastrointestinal tract may occasionally be detected by brush cytology but not seen in biopsie.s. Furthermore, the brush ranges over a wider area than that examined by biopsy, and cytologic specimens may be rapidly evaluated. Brush cytology has been shown to improve the diagnostic yield by 10% or more in some forms of gastrointestinal cancer in humans. 4 A tentative diagnosis made by brush cytology should not be summarily dismissed if not supported by biopsy results. Instead, repeated biopsies may be prudent. Aspiration of Duodenal Fluid Acquisition of duodenal fluid for culture and cytology is facilitated by the use of aspiration kits (Harford Veterinary Supply Co., Potomac, MD), consisting of a stylet and sterilized plastic tubing. Quantitative culture of duodenal fluid is an effective way to diagnose bacterial overgrowth of the small intestine. 1 Cytology of duodenal fluid is an accurate technique for the diagnosis of giardiasis. 10 Endoscopic Biopsy
Pinch Biopsy. Pinch biopsies are small (2 to 3 mm) biopsies that are attained by endoscopic guidance. In view of their small size, good technique is essential to acquire tissue samples of diagnostic value. The instrument must be sharp to avoid crush artifacts. Where possible, the long axis of the biopsy instrument should be directed at a 90-degree angle to the mucosal surface to be sampled. Pressure should be applied to the forceps so that they "bow" prior to clamping down to secure the biopsy. This lessens the likelihood of obtaining only surface cells, a common result if the biopsy forceps are directed parallel to the mucosal surface and not seated deeply.
UPPER GASTROINTESTINAL ENDOSCOPY
1221
In tubular lumens such as the small bowel, attaining a perpendicular orientation with the biopsy forceps is easier if the tip of the endoscope is extended until it encounters a flexure, or if the bowel is partially collapsed by the aspiration of the majority of luminal air. It can be useful to obtain more than one pinch biopsy from the same site to increase the depth of the tissue sampled. This is particularly important when obtaining biopsies of masses because of the inflammatory reaction that commonly surrounds neoplasms. Collapsing an organ by aspiration of luminal air, as well as choosing biopsy forceps with larger cups, will also allow for deeper biopsies. Biopsy of ulcerating lesions is best performed at their periphery to avoid the sampling of necrotic tissue. Because histologic anatomy varies within regions of the bowel, obtaining biopsies at consistent sites is likely to improve the ability of pathologists to differentiate normal from abnormal histology. For this reason, it has been suggested that as routine practice during upper GI endoscopy, biopsies should be obtained from any visible lesions and from the duodenum, pylorus, incisura angularis, mid greater curvature, and cardia. 7 At each site a minimum of three to four biopsies is suggested. If the pylorus cannot be negotiated, it is possible to obtain duodenal biopsies in a "blind" manner by passing the biopsy forceps through the pylorus while the endoscopic tip remains in the antrum. Suction Biopsy. The Quinton suction biopsy instrument is a safe and effective technique for attaining mucosal tissue from the esophagus. It is best suited for nontargeted biopsy of diffusely diseased tissue but, if the suction instrument is passed alongside the endoscope, targeted biopsies can occasionally be obtained. Handling of Biopsies. Endoscopic biopsy procedures yield pieces of tissue that are small and easily damaged. They should be handled gently, should not be allowed to dry, and should be placed on or in some support such as a piece of folded coverslip paper to minimize contraction and preserve orientation. For the best interpretation of biopsies, one should consult with the pathologist before the procedure about special biopsy requirements. Discordance of Biopsy Results and Clinical Signs. Discordant results among clinical signs, endoscopic examination, and biopsy studies are sometimes observed. For the clinician, it is most disturbing to receive a normal biopsy report when the clinical signs are suggestive of significant GI disease. The reasons for discordance have not been systematically examined. Some suggested causes are provided in Table 4. Discordance between biopsy results and endoscopic findings is also not uncommon. The concordance between endoscopic examination of the upper GI tract and biopsy results in dogs and cats has been the subject of a recent investigation. 7 In about two thirds of cases endoscopic abnormalities were associated with histologic abnormalities. Endoscopically observed mucosal hemorrhage and erythema held the least predictive value for histologic abnormality. Excess mucosal friability was associated with histologic abnormality in 80% of cases. The most obvious reasons for discordance are inexperienced clinicians, endoscopists, and pathologists. Other explanations are also possible, however, and include the presence of functional rather than morphologic bowel diseases, patchy distribution of mucosal lesions, and failure to
1222
W.
GRANT GUILFORD
Table 4. Reasons for Discordance of Biopsy Results with Clinical and Endoscopic Findings Incorrect localization of disease process by clinician Failure to separate large and small bowel diarrheas Incorrect endoscopic assessment of GI mucosa Inexperience Inadequate insufflation misread as mucosal thickening, mucosal granularity, or obscured submucosal blood vessels Scope-induced trauma misread as spontaneous·tlisease Incorrect biopsy evaluation by pathologist Inexperience The unknown significance of mild inflammation Sample handling error Nonrepresentative biopsies Poor biopsy technique Sampled incorrect aspect of a lesion (e.g., necrotic center) Patchy mucosal lesions Presence of functional rather than morphologic disease Brush-border defects Motility abnormalities Secretory diarrheas Permeability defects
From Strombeck DR, Guilford WG: Small Animal Gastroenterology, ed 2. Davis, CA, Stonegate Publishing, 1990; with permission.
place sufficient significance on mild morphologic change. The best example of the latter situation is provided by microscopic colitis of humans, a syndrome in which minimal histologic inflammation of the colon is associated with marked colonic dysfunction. 2 Post-treatment Biopsies. Some veterinarians recommend follow-up biopsies of the intestinal mucosa of all patients with moderate to severe inflammatory bowel disease. We have found follow-up biopsies to be helpful in those patients whose clinical signs are not responsive to therapy, given that they provide an objective assessment of the response of the intestinal inflammation to the therapeutic regimen. Clinically nonresponsive patients whose follow-up intestinal biopsies show a reduction in inflammation are maintained on the same therapy, and the client is instructed to allow more time for the disease to resolve. Clinically nonresponsive patients whose biopsies show no improvement are changed to a different therapeutic protocol, usually involving another controlled diet and more aggressive immunosuppression. The question of whether it is justified to collect a second biopsy in patients in clinical remission cannot as yet be answered. There is no doubt that many of these patients have evidence of persistent intestinal inflammation in spite of clinical remission. It is not uncommon for patients with subclinical GI inflammation to have a rapid recurrence of their clinical signs after the conclusion of the medical therapy. Moreover, it is quite conceivable that in the long-term this residual inflammation will lead to intestinal fibrosis and eventually a recurrence of untreatable clinical signs. Whether this theoretical concern justifies the expense of repeated intestinal biopsy can only be determined by carefully controlled prospective studies.
UPPER GASTROINTESTINAL ENDOSCOPY
1223
Foreign Body Retrieval Indications for Endoscopic Foreign Body Removal. Foreign bodies may be managed by conservative, endoscopic, or surgical means. Factors that influence this decision include the type of foreign object and its anatomic location, the clinical appearance of the animal, and the attentiveness with which the pet is observed by the owner. Careful survey radiographic evaluation of the patient prior to endoscopy is recommended. Radiography assists localization of the foreign body and the detection of perforation. When sharp objects such as fish hooks are observed by radiography, the veterinarian should carefully ascertain whether the foreign body remains in the lumen of the GI tract. Not uncommonly, sharp objects will penetrate the esophageal or GI wall where they become inaccessible to the endoscope. All esophageal foreign bodies (Fig. 9) should be rapidly removed, because they cause pain and dysphagia, and may result in esophageal stricture. Endoscopic removal is particularly desirable in view of the possible complications of esophageal surgery and thoracotomy. Timely endoscopic removal of all sharp objects from the stomach is recommended because of the risk of perforation of the stomach or, should the object leave the stomach, perforation of the intestine. To avoid GI obstruction, the early endoscopic or surgical removal of foreign bodies judged too large to pass through the GI tract is suggested. Foreign bodies suspected of containing lead, zinc (such as pennies, Fig. 10), or caustic materials (batteries) must be removed from the GI tract immediately. Technique. Successful retrieval of foreign bodies requires considerable discretion, ingenuity, and technical prowess. Tightly wedged foreign bodies should never be forcibly removed. If a foreign object cannot be removed by firm traction under direct endoscopic vision, then surgical removal is indicated. Forceful removal bears a great risk of laceration of the viscus or
Figure 9. Esophageal foreign body. This 5-year-old dachshund was presented with regurgitation. Esophagoscopy revealed a chewtoy wedged in the esophagus. (Courtesy of Dr. Sherri Wilson, University of California, Davis, Veterinary Medical Teaching Hospital.)
1224
w.
GRANT GUILFORD
Figure 10. Gastric foreign body. Three-prong grasping forceps are extended to grasp a penny that is lying at the junction of the gastric body and pyloric antrum. (Courtesy of Dr. Tullia Tonachini, University of California, Davis, Veterinary Medical Teaching Hospital.)
adjacent vessels or organs. Furthermore, tightly wedged foreign bodies usually have caused significant mucosal pressure necrosis that requires surgical inspection to determine its mural extent. Trial and error often determine the best retrieval instrument for a particular retrieval; however, certain generalizations may be made. For instance, basket retrieval instruments are only useful in a lumen of sufficient diameter to allow their expansion. Pronged graspers are of little value in the retrieval of foreign bodies with smooth surfaces. If the surface is smooth but indentable, strong jaw-tooth graspers are usually effective. Certain metals may be retrieved by magnetic extractors. Additional, useful retrieval techniques include entrapping the foreign body with suture material and then drawing the foreign body orally by traction on the suture material; pulling esophageal foreign bodies into a preplaced rigid tube in the esophagus, thus aiding atraumatic removal of sharp objects; pushing obstinate esophageal foreign bodies into the stomach where they may be digested (e.g., bones), better manipulated to an appropriate orientation for removal, or more easily removed surgically; and placing a Foley catheter distal to the object, then using the inflated catheter to draw the foreign body out. Bougienage Endoscopy assists the clinician to perform safe and effective esophageal bougienage. The endoscope allows visual assessment and biopsy of strictures before bougienage. This helps differentiate post-inflammatory strictures, extraesophageal compressions, and strictures resulting from neoplasia, thus facilitating the selection of an appropriate therapy. Furthermore, endoscopy simplifies the placement of the bougie directly into the orifice of the stricture and allows assessment of the effect of the procedure on the mucosal tissue and luminal diameter. Current evidence favors the use of balloon
UPPER GASTROINTESTINAL ENDOSCOPY
1225
bougienage. 3 The technique is simple, relying on gradual inflation of the balloon under fluoroscopic (contrast media-filled balloon) or endoscopic visualization. Manometers can be purchased to estimate pressures applied, but are not essential. Rigid bougies are used by systematically increasing the diameter of the bougie passed through the stricture. The stricture is dilated as widely as possible without the use of excessive force. The diameter of the largest bougie that is accommodated helps judge the success of the procedure. As an example, the comfortable passage of a 40 French diameter bougie through an esophageal stricture of a 20-kg dog would suggest adequate bougienage. Complications of bougienage include perforation of friable esophageal tissues and the rupture of major periesophageal vessels entrapped by the inflammatory or neoplastic disease process that formed the stricture. Endoscopic Placement of Gastrostomy Tubes Endoscopic placement of a gastrostomy tube is indicated for long-term (weeks to months) nutritional support of anorectic or dysphagic animals. Gastrostomy tubes are not recommended in vomiting animals. They are better tolerated than pharyngotomy or nasogastric tubes and can be easily managed at home. They are of comparatively large diameter and thus allow the economic use of blended pet foods and the direct administration of medicines. Complications are rare, but include pressure necrosis of the gastric wall or failure of gastroabdominal adhesion, both of which can result in peritonitis. An increased risk of peritonitis owing to failure of gastroabdominal adhesion following endoscopic placement of gastrostomy tubes has been noted in large, debilitated dogs undergoing chemotherapy (R. C. Straw, personal communication, 1989). Gastrostomy tubes in such patients may be better placed surgically. Endoscopic placement of gastrostomy tubes necessitates a brief anesthesia. Two techniques are in use, a percutaneous technique and a percutaneous-peroral technique. In both techniques, the animal is placed in right lateral recumbency so that the stomach tube may be placed through the greater curvature of the stomach and the left body wall. The site of emergence for the catheter should be just ventral to the 13th rib. The percutaneous-peroral technique has been described elsewhere.8 Technique. The percutaneous-peroral technique is the most commonly used technique for the endoscopic placement of gastrostomy tubes in veterinary patients. A specially prepared Pezzer mushroom-tipped catheter (Bard, Beneda, CA) or Malecot catheter is used for this procedure. A suitably sized catheter for dogs is 24 French and for cats, 20 French. Cut off 2 to 3 inches of the large diameter (female) end of the catheter and then trim the cut end of the catheter to facilitate its later introduction into the female end of a disposable plastic micropipette (MLA, Pleasantville, NY). Make a small slit in two 1- to 1.5-inch pieces of rubber tubing harvested from the 2- to 3-inch section of rubber that was previously cut from the mushroom catheter. These will serve as flanges to prevent movement of the stomach from the body wall. Pass the catheter through the slit in one of the flanges until the mushroom tip and the rubber flange are touching.
1226
W.
GRANT GUILFORD
Surgically prepare the left paracostal area centered just ventral to the distal end of the 13th rib. Introduce the endoscope into the stomach and carefully inflate this viscus until the abdomen is distended but not drum tight. Transilluminate with the endoscope to ensure the spleen is not between the stomach and body wall. Insert a 16- to 18-gauge, 1.5- to 2inch needle through the skin just ventral to the 13th rib and pass it through the body wall, gastric wall, and into the gastric lumen. Thread sturdy suture material, of sufficient length to reach from mouth to last rib, through the catheter into the lumen of the stomach. Grasp the suture with an endoscopic retrieval instrument and withdraw the endoscope from the animal, thus drawing one end of the suture through the esophagus and out of the mouth. Be careful not to draw all of the suture into the stomach. At the mouth, the suture material is then passed through the lumen of the plastic pipette (tapered end first) and firmly tied to the cut and trimmed end of the mushroom catheter. The catheter is then snugly wedged into the female end of the pipette. Grasp the suture material at its point of exit from the abdominal wall and apply firm traction to draw the entire catheter assemblage (pipette first) through the lumen of the mouth, esophagus, and stomach, and partially through the stomach and body wall. Further gentle traction on the catheter results in the distal (flanged) end of the catheter drawing the stomach wall against the body wall. It is anchored in this position by the second flange placed over the catheter at the skin surface. Bandage the catheter in place to prevent vandalism by the patient. After 6 to 7 days the catheter may be safely withdrawn. To remove the catheter, apply firm external traction and then cut the catheter as close to the distal tip as possible. The internal flange and mushroom tip usually pass uneventfully. The second technique for placement of gastrostomy tubes by endoscopy is the "percutaneous" technique. This technique uses a wire guide and a trocar and peel-away sheath that are serially passed through the abdominal wall into the air-distended stomach (PEG set, Wilson-Cook, WinstonSalem, NC). After penetration of the stomach, the wire guide and trocar are removed, and a lubricated Foley catheter is passed directly into the stomach through the peel-away sheath. Once the Foley catheter is inflated, the sheath is peeled away and pressure is carefully applied to the inflated Foley catheter to draw the stomach against the body wall. Both of these techniques have been successfully used at the University of California, Davis, Veterinary Medical Teaching Hospital. The percutaneous technique has a slightly shorter operating time, avoids contamination of the abdomen with oropharyngeal secretions, the female end of the catheter need not be cut off, and the removal process does not leave any flanges in the GI tract. Its disadvantages in comparison with the percutaneous-peroral technique include a less secure initial bond of the stomach to the body wall (the Foley balloon can rupture within 3 days) and greater expense for the PEG tray. Wilson-Cook will sell the component parts of the PEG tray separately, however, halving the list price. SUMMA:a.Y Upper GI endoscopy is a frequently performed endoscopic procedure that is particularly suited for the diagnosis of upper GI diseases with a
UPPER GASTROINTESTINAL ENDOSCOPY
1227
luminal or mucosal location. Contraindications are few and complications are rare. Procedures that can be performed during upper GI endoscopy include mucosal biopsy, brush cytology, aspiration of duodenal fluid for culture and cytology, foreign body retrieval, bougienage of strictures, and endoscopic placement of gastrostomy tubes. Unresolved issues that face veterinary endoscopists include the interrelationship between contrast radiology and endoscopy, the advisability of routine combination of upper and lower GI endoscopy, the reasons for discordance among clinical signs, endoscopic appearance, and biopsy findings, and the role of post-treatment biopsies.
REFERENCES 1. Batt RM, Needham JR, Carter MW: Bacterial overgrowth associated with a naturally occurring enteropathy in the German shepherd dog. Res Vet Sci 35:42, 1983 2. Bo-Linn GW, Vendrell DD, Lee E , eta!: An evaluation of the significance of microscopic colitis in patients with chronic diarrhea. J Clin Invest 75:1559, 1985 3. Burk RL, Zawie DA, Garvey MS: Balloon catheter dilation of intramural esophageal strictures in the dog and cat: A description of the procedure and a report of six cases. Semin Vet Med Surg 2:241, 1987 4. Halter F, Witzel L, Gretillat PA, et a!: Diagnostic value of biopsy, guided lavage, and brush cytology in esophagogastroscopy. Dig Dis 22:129, 1977 5. Jaffe JH, Martin WR: Opioid analgesics and antagonists. In Goodman Gilman A, Goodman LS, Rail TW, eta! (eds): The Pharmacological Basis of Therapeutics, ed 7. New York, MacMillan, 1985, p 502 6. Jakovljevic S: Gastric radiology and gastroscopy in the dog. Vet Ann 28:172, 1988 7. Leib MS, Roth L: Gastrointestinal endoscopy: Endoscopic and histologic correlation. Proceedings of the 7th ACVIM Forum, 1989, p 784 8. Mathews KA, Binnington AG: Percutaneous incisionless placement of a gastrostomy tube utilizing a gastroscope: Preliminary observations. J Am Anim Hosp Assoc 22:601, 1986 9. Pariente EA, Kerlau M, Lanoe JL, eta!: Fibroscopie ou radiographie oeso-gastroduodenale de premiere intention? Une evaluation pragmatique. Nouv Press Med 10:3477, 1981 10. Roudebush P, Delivorias MH: Duodenal aspiration via flexible endoscope for the diagnosis of giardiasis in a dog. JAm Vet Med Assoc 187:162, 1985
Address reprint requests to W. Grant Guilford, BVSc, BPhil Veterinary Medical Teaching Hospital School of Veterinary Medicine University of California, Davis Davis, CA 95616
0195-5616/90 $0.00
+ .20
Upper Gastrointestinal Endoscopy W. Grant Guilford, BVSc, BPhil*
Upper gastrointestinal (GI) endoscopy is the most frequently performed GI endoscopic procedure at the University of California, Davis, Veterinary Medical Teaching Hospital (Fig. 1). Upper GI endoscopy is a relatively noninvasive, atraumatic technique that permits visual examination of esophageal, gastric, and upper small bowel lesions and allows descriptive or photographic documentation of their severity and extent. Endoscopy provides biopsy, cytology, and fluid samples for laboratory evaluation. It allows therapeutic interventions such as foreign body retrieval, bougienage, and gastrostomy tube placement. It has a low morbidity and mortality but should only be used after routine work-up has failed to reveal a diagnosis.
INDICATIONS AND LIMITATIONS Upper GI endoscopy is most useful for the diagnosis of esophageal, gastric, and upper small intestinal disorders with a mucosal or luminal location. Lesions located in the muscular and submucosal layers of the bowel are more difficult to detect with an endoscope. Endoscopy and endoscopic biopsy ~etects morphologic but not functional disease. It will not detect abnormal GI motility, GI hypersecretory disorders, and subcellular defects such as brush border enzyme deficiencies. Because of restricted working length, current endoscopes cannot be used to evaluate mid-small intestinal disease. The clinical problems commonly evaluated by upper GI endoscopy are listed in Table 1. Upper Gastrointestinal Endoscopy Versus Contrast Radiography Upper GI contrast radiography and endoscopy are complementary procedures. Endoscopy is more sensitive for the diagnosis of mucosal diseases of the upper GI tract, and offers the important advantage of *Diplomate, American College of Veterinary Internal Medicine; Member, Small Animal Medicine Service, Veterinary Medical Teaching Hospital, and Research Fellow, Department of Physiological Sciences, University of California School of Veterinary Medicine, Davis, California Veterinary Clinics of North Am£rica: Small Animal Practice-Vol. 20, No. 5, September 1990
1209
1210
W.
Rhinoscopy
Bronchoscopy
24%
22%
GRANT GUILFORD
Figure l. Relative frequency of the different endoscopic procedures performed on 948 cats and dogs at University of California, Davis, Veterinary Medical Teaching Hospital. The miscellaneous category includes laryngoscopy, vaginoscopy, urethroscopy, laparoscopy, and thoracoscopy procedures. (From Strombeck DR, Guilford WG: Small Animal Gastroenterology, ed 2. Davis, CA, Stonegate Publishing, 1990; with permission.)
definitive diagnosis through tissue collection (cytology and biopsy). Contrast procedures do not require anesthesia, and they provide a better estimation of luminal diameter (esophagus), mural masses, extramural compressive lesions, jejunal diseases, GI motility, and gastric emptying. The prime function of the esophagus is one of motility. Disordered motility from esophageal neuromuscular disease is the most common cause Table 1. Principal Indications for Upper Gastrointestinal Endoscopy Evaluation of dysphagia Evaluation of regurgitation Evaluation of chronic vomiting Evaluation of hematemesis Evaluation of melena Evaluation of chronic diarrhea Retrieval of esophageal foreign bodies Bougienage of esophageal strictures Retrieval of select gastric foreign bodies Placement of percutaneous gastrostomy tubes
UPPER GASTROINTESTINAL ENDOSCOPY
1211
of esophageal dysfunction. Therefore, in most cases of suspected esophageal disease, barium swallows, preferably with fluoroscopy, are performed before endoscopy. The principal functions of the stomach and intestine are motility, secretion, and assimilation. Most disease processes that perturb these functions have a morphologic basis. Radiography is less sensitive than endoscopy for the detection of morphologic disease of the stomach in the dog. 6 Furthermore, radiography can localize morphologic disease, but can rarely define its cause. Therefore, in most cases of suspected gastroduodenal disease, endoscopic examination should precede contrast radiographic procedures. When endoscopy was used prior to contrast radiography for the diagnosis of suspected upper GI disease in a series of human patients, only 5% of the persons subsequently required barium studies. In comparison, when contrast radiography was the first procedure, 30% of the patients subsequently required endoscopy. 9 Combination Upper and Lower Gastrointestinal Endoscopy
It is the preference of some veterinary gastroenterologists to perform both gastroduodenoscopy and colonoscopy regardless of the character of the presenting signs. The endoscopic examination of the entire GI tract in one session has the advantage that subclinical disease in another part of the intestinal tract may be detected. This is particularly true of the inflammatory bowel diseases, disorders that do not respect the pylorus or ileocolic junction as an inviolate boundary. It is the preference of this author, however, to reserve the "hi-orifice" approach for patients that manifest signs of GI disease clearly referable to both large and small bowel dysfunction. The rational for this "uni-orifice" approach is that subclinical disease in another part of the GI tract only occasionally affects subsequent therapeutic approach or treatment success. In the opinion of this author, the extra expense and time involved in the "hi-orifice" approach is therefore rarely warranted. CONTRAINDICATIONS There are few absolute contraindications to performing GI endoscopy. The most common contraindication is patients that have an increased anesthetic risk. The procedure is not appropriate if bowel perforation is suspected, because contamination of the surrounding tissues may be increased as a result of the pressurization of the GI tract by air insuffiation. Endoscopy is discouraged in patients with inadequately prepared GI tracts, and in animals with bleeding diatheses.
COMPLICATIONS Complications of upper GI endoscopy are rare. Those most frequently encountered are listed in Table 2. Perforation of the esophagus with resultant mediastinitis and pleuritis or of the stomach or intestine with
1212
W.
GRANT GUILFORD
Table 2. Most Common Complications of Gastrointestinal Endoscopy GI perforation Laceration of major blood vessels Laceration of organs adjacent to the GI tract Decreased venous return owing to gastric overdistension Acute bradycardia Gastric·dilatation volvulus Mucosal hemorrhage Transmission of enteropathogenic organisms Bacteremias* *Incidence uncertain in veterinary medicine.
consequent peritonitis can result from forceful insertion of the endoscope, especially in the absence of vision of the lumen. Most commonly, however, perforation results from poor biopsy or retrieval technique. If a perforation is suspected, immediate radiography will usually confirm the diagnosis as large quantities of air rapidly escape the viscus to enter the surrounding body cavity. It can be difficult to detect the presence of small perforations by endoscopy. Gastric-dilatation-volvulus can occur following endoscopic procedures, perhaps owing to inadequate removal of insufflated air. Overdistension of the stomach with air during the procedure results in compression of the caudal vena cava and a rapid drop in venous return and blood pressure. Unless rapidly recognized and corrected, this is quickly fatal. Acute bradycardia, apparently due to vagovagal reflexes, can occur during endoscopy. This phenomenon most often occurs when the instrument enters the small intestine of small breeds and is perhaps caused by overdistension of the intestinal tract or by excessive traction on the mesentery. Major blood vessels can be ruptured during removal of foreign bodies and during bougienage. Rarely, considerable hemorrhage can follow biopsy procedures. Poorly disinfected scopes can transmit enteropathogenic organisms. Following routine endoscopy, oropharyngeal organisms can be transiently cultured from the blood of a small percentage of human patients. Whether the same phenomenon occurs in the· dog and cat is unknown.
PATIENT PREPARATION During the 12 to 24 hours prior to the endoscopic procedure, food should be withheld from the patient, and symptomatic therapy should be instituted to address any fluid or electrolyte abnormalities that may compromise anesthetic safety. Food should be withheld for a longer period if there is evidence of delayed gastric emptying. Retained gastric material interferes with visualization, may obstruct the operating/suction channel of the endoscope, and may result in pulmonary aspiration during anesthesia recovery. Anesthesia Anesthesia is essential for upper GI endoscopy. The anesthetic regimen chosen is de pendent on the animal's general condition and the presence of
UPPER GASTROINTESTINAL ENDOSCOPY
1213
any intercurrent disease. As a rule, inhalation anesthesia is used most frequently because of its safety and ease of administration. Anticholinergic premedication is an advantage to reduce gastric motility and secretion. Unfortunately, pyloric tone is not reduced by anticholinergics. Narcotics agents increase pyloric and cranial duodenal tone in humans, interfering with the easy passage of the scope. 5 The author's clinical impression is that a similar phenomenon occurs in dogs. Therefore, if the condition of the animal allows, thes€ drugs are best avoided during GI endoscopy. The anesthetist must be particularly alert for the signs of gastric overinflation, which include excessive abdominal distension, tachycardia, pale mucous membranes, and a precipitous drop in blood pressure, and for acute onset of bradycardia suggestive of vagovagal reflexes. Patient Positioning For routine upper GI endoscopy the patient is positioned in left lateral recumbency. This allows gastric juices to gravitate to the left side, away from the pyloric antrum and pylorus, and facilitates insufflation of the antrum. For the placement of gastrostomy tubes, the patient should be placed in right lateral recumbency. A reliable gag must always be placed in the mouth to protect the endoscope.
ENDOSCOPIC EXAMINATION Description of the Mucosa Written description of the mucosa should become part of the record of any animal undergoing endoscopy. Where appropriate, photographic records can also be kept. Consistent description of mucosal lesions is assisted by the preparation of endoscopy grading sheets for inclusion in the record. Grading sheets should include a description of the size and position of any lesions such as masses or ulcers. In addition, each of the following parameters should be evaluated in a semiquantitative fashion: degree of mucosal erythema, friability, granularity, and erosions; the amount of mucus; and the visibility of submucosal blood vessels. Of these parameters, increased mucosal erythema is least likely to correlate closely to the presence of mucosal disease. The appearance of the mucosa varies considerably with degree of insufflation. Esophagoscopy Flexible endoscopes allow the most thorough examination of the esophagus but rigid endoscopes can be used and may have some advantages in the removal of sharp foreign bodies. The endoscope is directed through the upper esophageal sphincter and the esophagus insufflated with air until sufficiently distended to visualize the lumen. The tip of the endoscope is then slowly advanced to the gastroesophageal junction. There may be a redundancy of tissue at the thoracic inlet that gives the impression of a diverticulum, but that can usually be largely obliterated by full extension
1214
W.
GRANT GUILFORD
Figure 2. Normal gastroesophageal junction.
of the neck. Pulsations of the esophagus will be present as one passes the endoscope over the heart. The normal mucosa is pale and smooth. Submucosal vessels are usually not visible. The luminal diameter of the esophagus can be hard to judge by endoscopy. In the anesthetized animal the normal esophagus appears flaccid and may partially drape over thoracic vasculature. For these reasons, be wary of diagnosing megaesophagus based on endoscopic judgment only. The gastroesophageal junction has a slit-like appearance (Fig. 2). Slight
Figure 3. Gastroesophageal junction of a 2-year-old rottweiler with chronic and severe esophagitis. Note the prominent mucosal irregularity. (Courtesy of Dr. Kim Robertson, University of California, Davis, Veterinary Medical Teaching Hospital.)
UPPER GASTROINTESTINAL ENDOSCOPY
1215
reddening may be apparent at the gastroesophageal junction in normal animals. When present, esophagitis may or may not be visually apparent. If it is apparent, erythema, erosions, irregularity, and strictures may be seen (Fig. 3). Because of its durable epithelium and tubular shape, biopsy of the esophagus is more difficult than the biopsy of other parts of the GI tract. The Quinton (Quinton Instrument Co, Seattle, WA) suction biopsy instrument is the safest and most effective method to collect a biopsy from the esophagus. Gastroscopy Following examination of the esophagus, the endoscope is gently advanced through the gastroesophageal sphincter into the stomach. On entry into the stomach, the mucosa of the undistended stomach usually obstructs most of the field of vision until the stomach is sufficiently insuffiated. The first part of the stomach wall that is visualized is usually the junction of the fundus and body. The lesser curvature is characterized by fewer, straighter mucosal folds than the greater curvature. Slight deviation of the tip of the scope away from the mucosa will allow the endoscopist to obtain a panoramic view of the body of the stomach as it is inflating. The endoscopist should be cognizant of the readiness with which the stomach inflates and the rugal folds disappear. If the stomach does not inflate, consider the possibility that air is exiting the stomach via the esophagus (firmly occlude by digital pressure if necessary), that your equipment is not insufflating correctly, or that the stomach is unable to distend owing to extramural compression or an intramural lesion. Prominent rugal folds are usually due to ineffective insuffiation but hypertrophic gastropathy must be considered. Overdistension of the stomach should be avoided because it can impede venous return, decrease tidal volume, allow a "belly" to develop in the insertion tube that inhibits maneuverability of the endoscope, and increase antral and pyloric contraction frequency by way of the antral reflex, both of which make passage of the endoscope into the duodenum more difficult (Fig. 4). The large size of the stomach means that the endoscopist must develop a systematic approach to gastroscopy, otherwise lesions will be missed. Particular care should be taken to observe the fundus, cardia, and lesser curvature, all areas of the stomach easily overlooked if the tip of the endoscope is single-mindedly passed to the pylorus along the greater curvature. If fluid is retained in the stomach it usually pools in the fundus and greater curvature of the body. Pooled fluid assists identification of this area but inhibits visualization of the mucosa. Large volumes of retained fluid should be aspirated to facilitate mucosal examination and to prevent aspiration during recovery. The incisura angularis is an important landmark (Fig. 5). It is a narrow shelf of tissue that divides the pyloric antrum from the lesser curvature of the gastric body. Because the natural progression of an aborally directed endoscope is along the greater curvature of the stomach, it is often necessary to retroflex the tip of the endoscope firmly by up to 180 degrees away from
w.
1216
GRANT GUILFORD
Decreased tidal volume Lungs Initiation of the antral reflex Increased antral and pyloric contractility
Inability to pass endoscope into pylorus Endoscope "belly"
I Figure 4. Consequences of gastric overdistention. Gastric overdistention results in a "belly" in the insertion tube of the endoscope, which inhibits maneuverability, increases antral contractions and pyloric tone, and compromises venous return and tidal volume. (From Strombeck DR, Guilford WG: Small Animal Gastroenterology, ed 2. Davis, CA, Stonegate Publishing, 1990; with permission.)
the greater curvature to obtain an en face view of the incisura. Once the incisura is identified, the pyloric antrum will be seen on one side and the lesser curvature, with the cardia dimly identifiable in the distance, will be seen on the other side. The cardia is easily identified by the presence of the insertion tube of the endoscope (Fig. 6). Once in the antrum, the tip of the endoscope is slowly advanced toward the pylorus. Movement of the scope into and along the antrum is inhibited if the stomach is overdistended. During this part of the examination, be sure that the lesser curvature of the pylorus is examined closely because lesibns can be easily missed in this area, especially when using scopes with narrow angles of view. The normal pylorus will usually yield to gentle pressure and allow entry of the tip of the endoscope into the duodenum. If not, the normal pylorus may be relaxed with glucagon (0.05 mg/kg, not to exceed 1 mg, IV). In some animals glucagon will induce a pronounced tachycardia. Adroit manipulation of the endoscope is often necessary to penetrate the pylorus. The normal stomach mucosa is bright pink to red and is lighter in color in the pyloric region. There should be no evidence of erosions or
UPPER GASTROINTESTINAL ENDOSCOPY
1217
Figure 5. Close-up of the incisura angularis of the stomach. The incisura is an important landmark: It divides the lesser curvature and cardia (top left) from the pyloric antrum (bottom right).
friability, suggestive of gastritis, or any indication of submucosal vessels (with the exception of the cardia or overdistended stomachs). The observation of submucosal vessels suggests a diagnosis of atrophic gastritis. Broad areas of induration in association with mucosal erosion or ulceration are usually a result of gastric cancer (Color Plate A). In hypertrophic gastropathy, the rugae often appear thickened and strongly light reflective, suggestive of edema. Furthermore, the rugal hypertrophy may be focal, and the folds may extend into the antrum, where
Figure 6. Gastric cardia. The cardia is easily identified by the presence of the insertion tube of the endoscope.
1218
W. GRANT GUILFORD
Figure 7. Normal pylorus. The incisura angularis of the stomach is visible at the top right of the figure. Foam adheres about the pyloric antrum.
it is unusual in normal animals to find many rugae. Mucosal erosions or ulcers may be apparent. The pylorus of normal dogs has a wide variety of appearances (Fig. 7). In general it should have clean margins, should not be obscured by excessive folds, and usually demonstrates rhythmical opening and closing. Occasionally, gastroduodenal reflux will be noticed. This is a normal occurrence in many dogs and cats. A patient with a hypertrophic pylorus will have a history compatible with delayed gastric emptying, may have retained gastric ingesta, evidence of rugal hypertrophy and mucosal erosions (hypergastrinemia owing to chronic distension), and usually has an enlarged, muscularlooking, protuberant pylorus with a small pyloric canal that is unable to accommodate the scope (Fig. 8). Some common problems encountered by inexperienced endoscopists during gastric examination and some suggested remedies are listed in Table 3. Duodenoscopy
After passage through the pylorus, the endoscope enters the short cranial duodenum and immediately encounters the cranial duodenal flexure . This is a very acute flexure that can be difficult to negotiate. It arises because of the rapid change of the cranial-and-to-the-right angulation of the pylorus and cranial duodenum to the caudal orientation of the descending duodenum. To negotiate this flexure . it is often necessary to flex the endoscope tip maximally, torque the insertion tube, and use a slide-by technique. Torquing the instrument at this point will be difficult if there is excess "belly" in the insertion tube as it rounds the greater curvature. The normal duodenal mucosa has a velvety appearance and a slightly more granular and friable nature than the stomach. Submucosal vessels are
UPPER GASTROINTESTINAL ENDOSCOPY
1219
Figure 8. Pyloric hypertrophy. Note the protuberant and muscular appearance of this hypertrophic pylorus. (Courtesy of Dr. Brent Jones, University of Missouri.)
not usually apparent. Careful examination may reveal the duodenal papillae. Abnormal duodenal mucosa commonly develops a pronounced granularity and friability. Occasionally, circular patches of lipid-laden villi may be observed, which are characteristic of lymphangiectasia (Color Plate B). Completion of the Endoscopic Examination After the endoscope reaches its full working length, it is slowly retracted. Biopsies, brush cytology, and aspiration of fluid are undertaken as indicated. All air should be aspirated from the GI lumen before the endoscope is withdrawn. The animal should then be allowed to recover from anesthesia and closely observed for the complications discussed previously. ANCILLARY ENDOSCOPIC TECHNIQUES Brush Cytology Brush cytology is a useful adjunct to endoscopic biopsy. It should be performed prior to biopsy so that the cytologic specimen is not contaminated with blood from the biopsy site. It may improve diagnostic yield because
1220
W.
GRANT GUILFORD
Table 3. The Gastric Examination: Trouble Shooting Problem: Inability to visualize the gastric lumen Reason: Inadequate insuffiation. Can be due to rapid loss of air through the esophagus or pylorus; equipment failure, depression of aspiration button on the handpiece instead of or along with the insuffiation button; extragastric compression; gastric mural disease Remedy: Manually occlude the esophagus, check equipment function, continually depress insuffiation button to keep pace with rapid ongoing losses Problem: Pyloric antrum and pylorus in view but scope will not advance into the antrum or repeatedly "flips" over the angularis toward the cardia Reason: Gastric overdistension creating a belly in the endoscope Remedy: Withdraw scope to cardia, partially deflate stomach and try again Problem: Unable to negotiate pylorus Reasons: Increased pyloric tone owing to gastric overdistension, narcotic administration, etc.; lateral placement of the pylorus in the antrum; anatomic pyloric obstruction Remedy: Partially deflate stomach; torque endoscope to allow utilization of the maximum deflection capability; administer glucagon to reduce pyloric tone
superficial material that otherwise may be lost during processing is sampled. Thus, organisms such as protozoa that reside in the mucus of the gastrointestinal tract may occasionally be detected by brush cytology but not seen in biopsie.s. Furthermore, the brush ranges over a wider area than that examined by biopsy, and cytologic specimens may be rapidly evaluated. Brush cytology has been shown to improve the diagnostic yield by 10% or more in some forms of gastrointestinal cancer in humans. 4 A tentative diagnosis made by brush cytology should not be summarily dismissed if not supported by biopsy results. Instead, repeated biopsies may be prudent. Aspiration of Duodenal Fluid Acquisition of duodenal fluid for culture and cytology is facilitated by the use of aspiration kits (Harford Veterinary Supply Co., Potomac, MD), consisting of a stylet and sterilized plastic tubing. Quantitative culture of duodenal fluid is an effective way to diagnose bacterial overgrowth of the small intestine. 1 Cytology of duodenal fluid is an accurate technique for the diagnosis of giardiasis. 10 Endoscopic Biopsy
Pinch Biopsy. Pinch biopsies are small (2 to 3 mm) biopsies that are attained by endoscopic guidance. In view of their small size, good technique is essential to acquire tissue samples of diagnostic value. The instrument must be sharp to avoid crush artifacts. Where possible, the long axis of the biopsy instrument should be directed at a 90-degree angle to the mucosal surface to be sampled. Pressure should be applied to the forceps so that they "bow" prior to clamping down to secure the biopsy. This lessens the likelihood of obtaining only surface cells, a common result if the biopsy forceps are directed parallel to the mucosal surface and not seated deeply.
UPPER GASTROINTESTINAL ENDOSCOPY
1221
In tubular lumens such as the small bowel, attaining a perpendicular orientation with the biopsy forceps is easier if the tip of the endoscope is extended until it encounters a flexure, or if the bowel is partially collapsed by the aspiration of the majority of luminal air. It can be useful to obtain more than one pinch biopsy from the same site to increase the depth of the tissue sampled. This is particularly important when obtaining biopsies of masses because of the inflammatory reaction that commonly surrounds neoplasms. Collapsing an organ by aspiration of luminal air, as well as choosing biopsy forceps with larger cups, will also allow for deeper biopsies. Biopsy of ulcerating lesions is best performed at their periphery to avoid the sampling of necrotic tissue. Because histologic anatomy varies within regions of the bowel, obtaining biopsies at consistent sites is likely to improve the ability of pathologists to differentiate normal from abnormal histology. For this reason, it has been suggested that as routine practice during upper GI endoscopy, biopsies should be obtained from any visible lesions and from the duodenum, pylorus, incisura angularis, mid greater curvature, and cardia. 7 At each site a minimum of three to four biopsies is suggested. If the pylorus cannot be negotiated, it is possible to obtain duodenal biopsies in a "blind" manner by passing the biopsy forceps through the pylorus while the endoscopic tip remains in the antrum. Suction Biopsy. The Quinton suction biopsy instrument is a safe and effective technique for attaining mucosal tissue from the esophagus. It is best suited for nontargeted biopsy of diffusely diseased tissue but, if the suction instrument is passed alongside the endoscope, targeted biopsies can occasionally be obtained. Handling of Biopsies. Endoscopic biopsy procedures yield pieces of tissue that are small and easily damaged. They should be handled gently, should not be allowed to dry, and should be placed on or in some support such as a piece of folded coverslip paper to minimize contraction and preserve orientation. For the best interpretation of biopsies, one should consult with the pathologist before the procedure about special biopsy requirements. Discordance of Biopsy Results and Clinical Signs. Discordant results among clinical signs, endoscopic examination, and biopsy studies are sometimes observed. For the clinician, it is most disturbing to receive a normal biopsy report when the clinical signs are suggestive of significant GI disease. The reasons for discordance have not been systematically examined. Some suggested causes are provided in Table 4. Discordance between biopsy results and endoscopic findings is also not uncommon. The concordance between endoscopic examination of the upper GI tract and biopsy results in dogs and cats has been the subject of a recent investigation. 7 In about two thirds of cases endoscopic abnormalities were associated with histologic abnormalities. Endoscopically observed mucosal hemorrhage and erythema held the least predictive value for histologic abnormality. Excess mucosal friability was associated with histologic abnormality in 80% of cases. The most obvious reasons for discordance are inexperienced clinicians, endoscopists, and pathologists. Other explanations are also possible, however, and include the presence of functional rather than morphologic bowel diseases, patchy distribution of mucosal lesions, and failure to
1222
W.
GRANT GUILFORD
Table 4. Reasons for Discordance of Biopsy Results with Clinical and Endoscopic Findings Incorrect localization of disease process by clinician Failure to separate large and small bowel diarrheas Incorrect endoscopic assessment of GI mucosa Inexperience Inadequate insufflation misread as mucosal thickening, mucosal granularity, or obscured submucosal blood vessels Scope-induced trauma misread as spontaneous·tlisease Incorrect biopsy evaluation by pathologist Inexperience The unknown significance of mild inflammation Sample handling error Nonrepresentative biopsies Poor biopsy technique Sampled incorrect aspect of a lesion (e.g., necrotic center) Patchy mucosal lesions Presence of functional rather than morphologic disease Brush-border defects Motility abnormalities Secretory diarrheas Permeability defects
From Strombeck DR, Guilford WG: Small Animal Gastroenterology, ed 2. Davis, CA, Stonegate Publishing, 1990; with permission.
place sufficient significance on mild morphologic change. The best example of the latter situation is provided by microscopic colitis of humans, a syndrome in which minimal histologic inflammation of the colon is associated with marked colonic dysfunction. 2 Post-treatment Biopsies. Some veterinarians recommend follow-up biopsies of the intestinal mucosa of all patients with moderate to severe inflammatory bowel disease. We have found follow-up biopsies to be helpful in those patients whose clinical signs are not responsive to therapy, given that they provide an objective assessment of the response of the intestinal inflammation to the therapeutic regimen. Clinically nonresponsive patients whose follow-up intestinal biopsies show a reduction in inflammation are maintained on the same therapy, and the client is instructed to allow more time for the disease to resolve. Clinically nonresponsive patients whose biopsies show no improvement are changed to a different therapeutic protocol, usually involving another controlled diet and more aggressive immunosuppression. The question of whether it is justified to collect a second biopsy in patients in clinical remission cannot as yet be answered. There is no doubt that many of these patients have evidence of persistent intestinal inflammation in spite of clinical remission. It is not uncommon for patients with subclinical GI inflammation to have a rapid recurrence of their clinical signs after the conclusion of the medical therapy. Moreover, it is quite conceivable that in the long-term this residual inflammation will lead to intestinal fibrosis and eventually a recurrence of untreatable clinical signs. Whether this theoretical concern justifies the expense of repeated intestinal biopsy can only be determined by carefully controlled prospective studies.
UPPER GASTROINTESTINAL ENDOSCOPY
1223
Foreign Body Retrieval Indications for Endoscopic Foreign Body Removal. Foreign bodies may be managed by conservative, endoscopic, or surgical means. Factors that influence this decision include the type of foreign object and its anatomic location, the clinical appearance of the animal, and the attentiveness with which the pet is observed by the owner. Careful survey radiographic evaluation of the patient prior to endoscopy is recommended. Radiography assists localization of the foreign body and the detection of perforation. When sharp objects such as fish hooks are observed by radiography, the veterinarian should carefully ascertain whether the foreign body remains in the lumen of the GI tract. Not uncommonly, sharp objects will penetrate the esophageal or GI wall where they become inaccessible to the endoscope. All esophageal foreign bodies (Fig. 9) should be rapidly removed, because they cause pain and dysphagia, and may result in esophageal stricture. Endoscopic removal is particularly desirable in view of the possible complications of esophageal surgery and thoracotomy. Timely endoscopic removal of all sharp objects from the stomach is recommended because of the risk of perforation of the stomach or, should the object leave the stomach, perforation of the intestine. To avoid GI obstruction, the early endoscopic or surgical removal of foreign bodies judged too large to pass through the GI tract is suggested. Foreign bodies suspected of containing lead, zinc (such as pennies, Fig. 10), or caustic materials (batteries) must be removed from the GI tract immediately. Technique. Successful retrieval of foreign bodies requires considerable discretion, ingenuity, and technical prowess. Tightly wedged foreign bodies should never be forcibly removed. If a foreign object cannot be removed by firm traction under direct endoscopic vision, then surgical removal is indicated. Forceful removal bears a great risk of laceration of the viscus or
Figure 9. Esophageal foreign body. This 5-year-old dachshund was presented with regurgitation. Esophagoscopy revealed a chewtoy wedged in the esophagus. (Courtesy of Dr. Sherri Wilson, University of California, Davis, Veterinary Medical Teaching Hospital.)
1224
w.
GRANT GUILFORD
Figure 10. Gastric foreign body. Three-prong grasping forceps are extended to grasp a penny that is lying at the junction of the gastric body and pyloric antrum. (Courtesy of Dr. Tullia Tonachini, University of California, Davis, Veterinary Medical Teaching Hospital.)
adjacent vessels or organs. Furthermore, tightly wedged foreign bodies usually have caused significant mucosal pressure necrosis that requires surgical inspection to determine its mural extent. Trial and error often determine the best retrieval instrument for a particular retrieval; however, certain generalizations may be made. For instance, basket retrieval instruments are only useful in a lumen of sufficient diameter to allow their expansion. Pronged graspers are of little value in the retrieval of foreign bodies with smooth surfaces. If the surface is smooth but indentable, strong jaw-tooth graspers are usually effective. Certain metals may be retrieved by magnetic extractors. Additional, useful retrieval techniques include entrapping the foreign body with suture material and then drawing the foreign body orally by traction on the suture material; pulling esophageal foreign bodies into a preplaced rigid tube in the esophagus, thus aiding atraumatic removal of sharp objects; pushing obstinate esophageal foreign bodies into the stomach where they may be digested (e.g., bones), better manipulated to an appropriate orientation for removal, or more easily removed surgically; and placing a Foley catheter distal to the object, then using the inflated catheter to draw the foreign body out. Bougienage Endoscopy assists the clinician to perform safe and effective esophageal bougienage. The endoscope allows visual assessment and biopsy of strictures before bougienage. This helps differentiate post-inflammatory strictures, extraesophageal compressions, and strictures resulting from neoplasia, thus facilitating the selection of an appropriate therapy. Furthermore, endoscopy simplifies the placement of the bougie directly into the orifice of the stricture and allows assessment of the effect of the procedure on the mucosal tissue and luminal diameter. Current evidence favors the use of balloon
UPPER GASTROINTESTINAL ENDOSCOPY
1225
bougienage. 3 The technique is simple, relying on gradual inflation of the balloon under fluoroscopic (contrast media-filled balloon) or endoscopic visualization. Manometers can be purchased to estimate pressures applied, but are not essential. Rigid bougies are used by systematically increasing the diameter of the bougie passed through the stricture. The stricture is dilated as widely as possible without the use of excessive force. The diameter of the largest bougie that is accommodated helps judge the success of the procedure. As an example, the comfortable passage of a 40 French diameter bougie through an esophageal stricture of a 20-kg dog would suggest adequate bougienage. Complications of bougienage include perforation of friable esophageal tissues and the rupture of major periesophageal vessels entrapped by the inflammatory or neoplastic disease process that formed the stricture. Endoscopic Placement of Gastrostomy Tubes Endoscopic placement of a gastrostomy tube is indicated for long-term (weeks to months) nutritional support of anorectic or dysphagic animals. Gastrostomy tubes are not recommended in vomiting animals. They are better tolerated than pharyngotomy or nasogastric tubes and can be easily managed at home. They are of comparatively large diameter and thus allow the economic use of blended pet foods and the direct administration of medicines. Complications are rare, but include pressure necrosis of the gastric wall or failure of gastroabdominal adhesion, both of which can result in peritonitis. An increased risk of peritonitis owing to failure of gastroabdominal adhesion following endoscopic placement of gastrostomy tubes has been noted in large, debilitated dogs undergoing chemotherapy (R. C. Straw, personal communication, 1989). Gastrostomy tubes in such patients may be better placed surgically. Endoscopic placement of gastrostomy tubes necessitates a brief anesthesia. Two techniques are in use, a percutaneous technique and a percutaneous-peroral technique. In both techniques, the animal is placed in right lateral recumbency so that the stomach tube may be placed through the greater curvature of the stomach and the left body wall. The site of emergence for the catheter should be just ventral to the 13th rib. The percutaneous-peroral technique has been described elsewhere.8 Technique. The percutaneous-peroral technique is the most commonly used technique for the endoscopic placement of gastrostomy tubes in veterinary patients. A specially prepared Pezzer mushroom-tipped catheter (Bard, Beneda, CA) or Malecot catheter is used for this procedure. A suitably sized catheter for dogs is 24 French and for cats, 20 French. Cut off 2 to 3 inches of the large diameter (female) end of the catheter and then trim the cut end of the catheter to facilitate its later introduction into the female end of a disposable plastic micropipette (MLA, Pleasantville, NY). Make a small slit in two 1- to 1.5-inch pieces of rubber tubing harvested from the 2- to 3-inch section of rubber that was previously cut from the mushroom catheter. These will serve as flanges to prevent movement of the stomach from the body wall. Pass the catheter through the slit in one of the flanges until the mushroom tip and the rubber flange are touching.
1226
W.
GRANT GUILFORD
Surgically prepare the left paracostal area centered just ventral to the distal end of the 13th rib. Introduce the endoscope into the stomach and carefully inflate this viscus until the abdomen is distended but not drum tight. Transilluminate with the endoscope to ensure the spleen is not between the stomach and body wall. Insert a 16- to 18-gauge, 1.5- to 2inch needle through the skin just ventral to the 13th rib and pass it through the body wall, gastric wall, and into the gastric lumen. Thread sturdy suture material, of sufficient length to reach from mouth to last rib, through the catheter into the lumen of the stomach. Grasp the suture with an endoscopic retrieval instrument and withdraw the endoscope from the animal, thus drawing one end of the suture through the esophagus and out of the mouth. Be careful not to draw all of the suture into the stomach. At the mouth, the suture material is then passed through the lumen of the plastic pipette (tapered end first) and firmly tied to the cut and trimmed end of the mushroom catheter. The catheter is then snugly wedged into the female end of the pipette. Grasp the suture material at its point of exit from the abdominal wall and apply firm traction to draw the entire catheter assemblage (pipette first) through the lumen of the mouth, esophagus, and stomach, and partially through the stomach and body wall. Further gentle traction on the catheter results in the distal (flanged) end of the catheter drawing the stomach wall against the body wall. It is anchored in this position by the second flange placed over the catheter at the skin surface. Bandage the catheter in place to prevent vandalism by the patient. After 6 to 7 days the catheter may be safely withdrawn. To remove the catheter, apply firm external traction and then cut the catheter as close to the distal tip as possible. The internal flange and mushroom tip usually pass uneventfully. The second technique for placement of gastrostomy tubes by endoscopy is the "percutaneous" technique. This technique uses a wire guide and a trocar and peel-away sheath that are serially passed through the abdominal wall into the air-distended stomach (PEG set, Wilson-Cook, WinstonSalem, NC). After penetration of the stomach, the wire guide and trocar are removed, and a lubricated Foley catheter is passed directly into the stomach through the peel-away sheath. Once the Foley catheter is inflated, the sheath is peeled away and pressure is carefully applied to the inflated Foley catheter to draw the stomach against the body wall. Both of these techniques have been successfully used at the University of California, Davis, Veterinary Medical Teaching Hospital. The percutaneous technique has a slightly shorter operating time, avoids contamination of the abdomen with oropharyngeal secretions, the female end of the catheter need not be cut off, and the removal process does not leave any flanges in the GI tract. Its disadvantages in comparison with the percutaneous-peroral technique include a less secure initial bond of the stomach to the body wall (the Foley balloon can rupture within 3 days) and greater expense for the PEG tray. Wilson-Cook will sell the component parts of the PEG tray separately, however, halving the list price. SUMMA:a.Y Upper GI endoscopy is a frequently performed endoscopic procedure that is particularly suited for the diagnosis of upper GI diseases with a
UPPER GASTROINTESTINAL ENDOSCOPY
1227
luminal or mucosal location. Contraindications are few and complications are rare. Procedures that can be performed during upper GI endoscopy include mucosal biopsy, brush cytology, aspiration of duodenal fluid for culture and cytology, foreign body retrieval, bougienage of strictures, and endoscopic placement of gastrostomy tubes. Unresolved issues that face veterinary endoscopists include the interrelationship between contrast radiology and endoscopy, the advisability of routine combination of upper and lower GI endoscopy, the reasons for discordance among clinical signs, endoscopic appearance, and biopsy findings, and the role of post-treatment biopsies.
REFERENCES 1. Batt RM, Needham JR, Carter MW: Bacterial overgrowth associated with a naturally occurring enteropathy in the German shepherd dog. Res Vet Sci 35:42, 1983 2. Bo-Linn GW, Vendrell DD, Lee E , eta!: An evaluation of the significance of microscopic colitis in patients with chronic diarrhea. J Clin Invest 75:1559, 1985 3. Burk RL, Zawie DA, Garvey MS: Balloon catheter dilation of intramural esophageal strictures in the dog and cat: A description of the procedure and a report of six cases. Semin Vet Med Surg 2:241, 1987 4. Halter F, Witzel L, Gretillat PA, et a!: Diagnostic value of biopsy, guided lavage, and brush cytology in esophagogastroscopy. Dig Dis 22:129, 1977 5. Jaffe JH, Martin WR: Opioid analgesics and antagonists. In Goodman Gilman A, Goodman LS, Rail TW, eta! (eds): The Pharmacological Basis of Therapeutics, ed 7. New York, MacMillan, 1985, p 502 6. Jakovljevic S: Gastric radiology and gastroscopy in the dog. Vet Ann 28:172, 1988 7. Leib MS, Roth L: Gastrointestinal endoscopy: Endoscopic and histologic correlation. Proceedings of the 7th ACVIM Forum, 1989, p 784 8. Mathews KA, Binnington AG: Percutaneous incisionless placement of a gastrostomy tube utilizing a gastroscope: Preliminary observations. J Am Anim Hosp Assoc 22:601, 1986 9. Pariente EA, Kerlau M, Lanoe JL, eta!: Fibroscopie ou radiographie oeso-gastroduodenale de premiere intention? Une evaluation pragmatique. Nouv Press Med 10:3477, 1981 10. Roudebush P, Delivorias MH: Duodenal aspiration via flexible endoscope for the diagnosis of giardiasis in a dog. JAm Vet Med Assoc 187:162, 1985
Address reprint requests to W. Grant Guilford, BVSc, BPhil Veterinary Medical Teaching Hospital School of Veterinary Medicine University of California, Davis Davis, CA 95616
