0016-5107/87/3306-0427$02.00GASTROINTESTINAL ENDOSCOPYCopyright © 1987 by the American Society for Gastrointestinal Endoscopy

Can the use of an endoscopic Congo red testdecrease the incidence of incompleteproximal gastric vagotomy?

Philip E. Donahue, MD, Junichi Yoshida, MDHarry M. Richter, MD, C. Thomas Bombeck, MD

Lloyd M. Nyhus, MD, Dieter Maroske, MDKlaus P. Thon, MD, Hans D. Roeher, MD

Chicago, Illinois, and Marburg, West Germany

The endoscopic Congo red test allows accurate and rapid evaluation of thecompleteness of vagotomy and may result in a lower incidence of postoperativeincomplete vagotomy. This report describes 44 patients tested during proximalgastric vagotomy. Evidence of incomplete vagotomy was found in over 95% at theconclusion of the conventional operation. Importantly, the test was a guide tofurther operative maneuvers which abolished the evidence of incompletevagotomy upon subsequent testing. The endoscopic Congo red test satisfies therequirements for an ideal test for complete vagotomy: it is easily performed, doesnot require special equipment, and can be repeated several times if necessary toverify that desired effects have been achieved. The wider use of this test,therefore, appears justified. (Gastrointest Endosc 1987;33:427-431)

All physicians and surgeons recognize the seriousnature of some of the postoperative symptoms aftergastric resection or pyloroplasty. Indeed, many ofthese patients have been frequent visitors to the med­ical and surgical clinics in large medical centers andhave, by their demonstrated difficulties, helped en­courage the development of operations not associatedwith severe postoperative symptoms. With respect toduodenal ulcer surgery, proximal gastric vagotomy(PGV) has been proposed as an alternative to otheroperations with a high incidence of postoperativesymptoms. However, PGV has not been generallyaccepted in the United States because the risk ofrecurrent ulcerations, presumably due to incompletevagotomy of the parietal cell mass, is too high. Sincemost recurrent ulcers are caused by acid hypersecre­tion, intraoperative testing for completeness of vagot­omy holds promise as a way of improving postopera­tive results. We have previously described modifica­tions in the endoscopic Congo red test (ECRT) for

Received September 15, 1986. Accepted October 23, 1986.From the Deportments of Surgery, Cook County Hospital, the Uni­versity of IUinois, Chicago, and the Veterans Administration WestSide Medical Center, Chicago, Illinois; and the Philipps-UniversityKlinik, Marburg, West Germany. Reprint requests: Philip E. Dono­hue, MD, General Surgery, Room 2201, Cook County Hospital, 1835W. Harrison Street, Chicago, Illinois 60612.

VOLUME 33, NO.6, 1987

evaluating the completeness of vagotomy, 1 and we nowreport the results of its use during operations per­formed in two medical centers.

MATERIALS AND METHODS (TABLES 1 AND 2)

All patients with chronic duodenal ulcer had radiologicand endoscopic proof of chronic ulcer and had been refrac­tory to medical therapy for 6 months to 10 years prior tooperation. These patients had had episodes of pain alone(6), repeated episodes of bleeding (20), gastric outlet obstruc­tion (16), or perforation (2) as the indication for definitivetreatment of the ulcer disease. All ECRTs were done underthe supervision of one of the authors (P.E.D.), includingthose in Marburg during March 1986.

The ECRT utilizes the pH-sensitive indicator dye Congored to show differences in the relative rates of acid secretionbetween innervated and denervated gastric mucosa. Congored is red only when the pH is above 3.0; below pH 3.0, thedye is blue-black in color. If the stomach is washed withdilute bicarbonate solution and coated with the dye, the rateof color change is an indirect measure of the rate of acidsecretion. As acid is secreted, the Congo red dye solution(which is red at pH > 3.0 and black at pH < 3.0) turnsblack; portions of the stomach that were vagally denervatedremain alkaline (red) for 10 min or more, while those areasof the stomach with intact nerves exhibit a rapid colorchange.

When Congo red dye mixed with bicarbonate is applied

427

Table 1.Important technical details regarding the endoscopicCongo red test

1. The stomach must be free of food or vegetable debris.2. The Congo red and dilute bicarbonate solution are applied as a

single solution.3. The strength of the NaHC03 is varied at times; usually a 0.5%

mixture is used (intraoperatively). In the postoperative clinic, a5.0% solution is used.

4. Gastric secretion must be stimulated with pentagastrin at theusual dose of 6 /lg/kg when the patient is anesthetized.

5. When lavaging the stomach intraoperatively, the use of a largetube attached to the endoscope is preferable to spraying solutionsthrough the endoscope-biopsy port. The goal of the procedure isto coat the entire mucosal surface with the solution rapidly.

to an intact, unoperated stomach, the red-to-black colorchange is noted almost immediately. Following completevagotomy, 8 to 10 min elapse before the red-to-black colorchange is definite. Those patients with incomplete vagotomyhave a mixture of areas of the stomach with rapid colorchange (intact nerves) and areas with delayed color change.When the test is performed intraoperatively, the surgeoncan immediately try to complete the operative vagotomyand repeat the test to confirm that vagotomy of the parietalcell mass has been completed. Since the patient must besecreting acid during the test, a secretagogue such as pen­tagastrin is given prior to testing (6 JLg/kg/sc).

PGV was performed in accordance with accepted princi­ples for complete vagotomy, including extensive periesoph­ageal dissection and meticulous dissection of the lesser curveof the stomach.2

-4 The heel of the crow's foot and thegastropancreatic fold were carefully dissected in individualcases, and the nerves of the greater curvature were dividedif the first ECRT indicated incomplete vagotomy. Aftercompleting the division of residual neurovascular bundles assuggested by the first test, the ECRT was repeated a secondtime. The completed operative dissection is shown in Figures1 and 2.

RESULTS

A total of 44 patients were operated upon, including38 in Chicago and six at Marburg. In all cases theECRT was done near the completion of the conven­tional PGV. The test showed evidence of incompletevagotomy of the parietal cell mass in 42 of 44 (96%)patients. The most common areas of the stomach thatwere "positive" after the conventional PGV were areasof the greater curvature of the stomach and the lessercurve of the stomach near the antrum-corpus junction(Fig. 3).

The pattern of positivity along the greater curvewas of interest, since it could be abolished by divisionof the right and/or left gastroepiploic nerves. Thediscrete pattern varied widely, from a small patch ofblackened mucosa (less than 5.0% of the gastric mu­cosa) to very large blackened areas corresponding toalmost 60% of the parietal cell mucosa. The area ofthe distal greater curvature, however, was the mostpersistently positive (40 of the 42 positives), while the

428

Table 2.Steps in performing the endoscopic Congo red test

Intraoperative1. Prepare the patient by discontinuing anticholinergic/Hz-receptor

antagonists 24 hours prior to operation.2. Request that the anesthesiologist avoid, when possible, anticho­

linergic premedication.3. Prepare the endoscope (pediatric size preferable) and solutions:

• Check the air, water, and suction functions of the endoscope.• Endoscope must be free of stray electrical currents and be

properly grounded for use in the operating room.• Have several500-ml basins: one with saline solution, one with

0.5% NaHC03 (and one that can be used later for making a2.0% solution ifthe first test shows that a 0.5% solution cannotshow the difference between innervated and denervated mu­cosa).

• Add 3.0 g of Congo red powder to the 0.5% solution above andlabel.

• Have a no. 14-16 nasogastric tube and a 50-cc irrigating sy­ringe.

4. Have pentagastrin (6 /lg/kg) for subcutaneous injection 15 to 20min prior to performing the test.

5. Place the endoscope and light source at the head of the table;remove the esophageal stethoscope and nasogastric tube. Attachthe small nasogastric tube to the endoscope with three rubberbands 5 cm apart (nasogastric tube will facilitate rapid irrigationand aspiration of solution).!

6. Insert the endoscope; when difficult, ask the anesthetist to insertthe endoscope into the hypopharynx. The endoscopist the passesthe endoscope into the stomach under direct vision and assesseswhether a preliminary lavage (saline) is necessary to removedebris/mucus.

7. Have the gastroesophageal junction tethered with a catheter tominimize the risk of reflux of acidic solution into the esophagus;obturate the duodenum.

8. Inject 200 ml of 0.5% bicarbonate/Congo red solution via thenasogastric tube; have the assistant manipulate the stomach toensure coating of entire surface. Aspirate the stomach via thenasogastric tube and "plug" the tube. Look into the stomach toverify that the entire surface is either red or black: if so, proceedwith the test (note the time). If any of the mucosa is uncoatedwith redfblack solution, repeat the irrigation/aspiration se­quence.

9. Positive findings: Blackened areas are seen within 2 min (thered-to-black color change occurs as the pH falls below 3.0). Incontrast, denervated areas secrete acid slowly enough to delaythe color change for 8 to 10 min. If the test is ++, note area ofpositivity and search for intact nerve fibers before repeating thetest. If the entire stomach is black within 2 min (includingdenervated area), repeat lavage with a 2.0% bicarbonate/Congored mixture. Remember that the goal is to show a differentialrate of secretion between innervated and denervated mucosa andthat the final NaHC03 concentration is not critical.

Postoperative (ambulatory patients)1. Confirm suspicion of recurrent ulcer endoscopically.2. Have the patient discontinue all Hz-receptor antagonists the

evening before.3. Use minimal sedation (if any).4. Have materials for the test ready: (a) endoscope, and (b) solution

of 0.5% Congo red and 5.0% bicarbonate.5. Insert endoscope; aspirate any fluid in the stomach. Spray the

entire stomach with the mixture via an endoscopic sprayingdevice; begin the spraying distally.

6. Aspirate excess solution and note the time. Any area of thestomach that turns black within the first 2 to 3 min is consideredto have rapid acid secretion and is presumed to have intact vagusnerve innervation.

GASTROINTESTINAL ENDOSCOPY

more proximal stomach was positive in 15 instances;there was only one case in which the proximal stomachwas positive when the distal portion of the greatercurvature was negative. There were residual areasopposite the spleen in 13 of the 42 positives. Most ofthe area of residual positive reaction was abolished bydivision of the right and/or left gastroepiploic pedicle.On three occasions the right gastroepiploic nerve alonewas divided (instead of the entire neurovascular ped­icle) with the same result. We recommend division ofthe entire neurovascular pedicle, however, because thegastroepiploic nerve is often multiple and because itis easy to cause a hematoma when isolating the nerve.Those portions of the stomach opposite the spleenoften retained a positive reaction; the short gastric

Post trunk va\lus n , , , ,

Hepatic a.----~

R. gastric a.-/ .

Figure 1. The major blood vessels and nerves that supply thestomach. Note the position of the anterior and posteriorgastric nerves and the termination of these nerves on theantrum of the stomach. The terminal portion is called thenerve of Latarjet, and the point of insertion is referred to asthe "crow's foot."

pedicles, however, were not divided to avoid devascu­larization of the proximal stomach. (Technical note:Following the extended PGV, the stomach's blood isprovided mainly by the right gastric artery and theshort gastric arteries, possibly supplemented by anyintramural vessels which traverse the cardia or pyloricregions from esophagus and duodenum, respectively.)

Figure 2. The retractor and clamp at the lesser curve of thestomach indicate several small nerve branches at the "heel"of the "craw's foot" (the insertion of the Latarjet nerve hasthree branches, likened to the foot of a crow by Hedenstedt).These fibers innervate the distal part of the corpus andaccount for the positive areas along the lesser curve duringECRT. Clamp tips are shown at the approximate point atwhich division of the right and left gastroepiploic nerves isperformed.

Figure 3. The distal stomach as seen endoscopically during ECRT. Left, A positive spot on the greater curve of the stomach atthe antrum-eorpus junction (opposite incisura). Right, The findings of the second ECRT after the right gastroepiploic pedicle wasdivided; almost all of the blackened area indicative of rapid acid secretion has disappeared.

VOLUME 33, NO.6, 1987 429

DISCUSSION

Despite several theoretical advantages, the practiceof PGV has been marred by scientific and practicaldifficulties. The most notable of these is that the ulcerrecurrence rate following PGV is extremely variable,ranging from 2% to 30%.4-11 Therefore, many sur­geons, especially those in the United States, believethe operation is simply not effective enough to be usedroutinely. In addition, experienced surgeons are con­cerned that the anatomic endpoints for completion ofoperative dissection during PGV are unclear, leadingto obvious great variability in the way the operationis performed in different medical centers.12.13 Last,and perhaps not surprising, gastric secretory studiesshow that PGV has a highly variable effect on post­operative acid secretion, resulting in a 30% to 85%decrease in acid secretion.14 Before PGV can becomethe operation of choice, surgeons and referring physi­cians must be assured that this procedure can reliablyreduce gastric acid secretion so that the primary goalof curing the duodenal ulcer can be achieved.

The technical description of the operations per­formed by those clinics reporting either the best orthe worst results after PGV seem to describe the sameoperation. However, the differences in recurrencerates suggest that different techniques are being em­ployed in the different medical centers. When observ­ing the operation of PGV in different medical centers,we have found subtle but real differences in the waythis operation is performed. We firmly believe thatfurther standardization of the technique of this oper­ation is a highly desirable goal, and that those physi­cians and surgeons who pursue gastrointestinal en­doscopy have a unique opportunity to participate inthis process. Intraoperative testing with the modifiedECRT suggests that the conventional PGV operationleaves variable portions of the stomach with a capacityfor rapid acid secretion. Furthermore, the evidencesuggests that some of the efferent vagal fibers to theparietal cell mass are being left undivided duringconventional PGV.12.13 These areas of persistent acidsecretion disappear following division of the gastro­epiploic nerve fibers that enter the greater curvatureof the stomach.

Interestingly enough, these areas that are resistantto denervation appear to be identical to those areasfound in clinics that employ intraoperative pH testingto demonstrate the immediate results of vagal nervesection.15.16 However, there has never been a system­atic demonstration that the nerves of the greatercurvature have a physiologic function.

The first clinical application of PGV was in theclinic of Holle4 in Munich in the early 1960s. Holleused PGV with a gastric drainage procedure tailoredto the anatomy of the individual patient. The recur­rence rate in his clinic, 1.1% of 1,347 patients followedfor 10 to 20 years, is one of the lowest rates ever

430

reported. Early application of the operation outsideGermany was limited to carefully defined study groupsbecause of concerns about the possibility of high re­currence rates-a concern found to be quite justified.

Following the report from England by Goligher in1974,2 surgeons in Great Britain and Europe recog­nized that branches of the vagus nerve surroundingthe distal esophagus could reach the stomach; incom­plete vagotomy due to these nerves was prevented byclearing the distal esophagus for a length of 5 to 7 emduring PGV. Clinics that adopted this approach wereable to improve their results after PGV, as shown byHallenbeck et aU7

Although the practical aspects of operative dissec­tion are usually limited to surgical journals or opera­tive texts, we believe that some of this informationcan be quite helpful to nonsurgeons as well as tosurgeons. It is desirable for all of us to have clear ideasabout the variations in operative technique that mightaffect postoperative function, and to appreciate theways in which we can evaluate the results of ourtherapy. Use of the ECRT allows both physicians andsurgeons to estimate the rate of acid secretion (and,hence, the probability that the vagus nerves are intact)in patients who have had any type of vagotomy pre­viously. While the remarks above have been directedat the evaluation of patients during PGV, we havealso applied this test successfully in patients withrecurrent ulcers following truncal vagotomy. TheECRT performed in the postoperative clinic has cor­rectly indicated the location of the intact nerve in90% of the cases in which patients have been operatedupon subsequently for completion of the truncal va­gotomy.

None of our findings provide conclusive evidencefor the hypothesis that the nerves of the greater cur­vature playa role in acid secretion, and that failure todivide these nerves will result in incomplete vagotomyof the parietal cell mass. We recognize that we mustobtain 5- to 10-year follow-up studies in the patientswho have had extended PGV to substantiate the claimthat this operation is more effective than the standardprocedure. Therefore, we are somewhat reluctant torecommend that all surgeons divide these nerves alongthe greater curvature during PGV. However, the visualECRT evidence of a 96% incomplete vagotomy ratefollowing the standard PGV seems to speak for itself.Use of the ECRT will improve the performance ofPGV in all medical centers if it leads staff membersto reevaluate all aspects of performance of this oper­ation. Also, the increased use of this test by physiciansand surgeons may increase our knowledge about theresults of current operative therapy and help us planmore effective surgical interventions in the future.

REFERENCES1. Donahue PE, Bombeck CT, Nyhus LM. The simplified endo­

scopic Congo red test for completeness of vagotomy. Surg

GASTROINTESTINAL ENDOSCOPY

Gynecol Obstet 1986;163:287-89.2. Goligher JC A technique for highly selective vagotomy for

duodenal ulcer. Br J Surg 1974;61:337-45.3. Griffith CA, Harkins HN. Partial gastric vagotomy: an experi­

mental study. Gastroenterology 1957;32:96-102.4. Holle FK. The physiologic background and standard technique

of selective proximal vagotomy with pyloroplasty. Surg GynecolObstet 1977;145:853-9.

5. Kennedy T, Johnston GW, Macrae KD, Spencer EFA. Proximalgastric vagotomy: interim results of a randomized controlledtrial. Br Med J 1975;2:301-3.

6. Kronborg 0, Jorgensen PM. Influence of different techniquesof PGV upon the risk of recurrent DU and gastric acid secretion.Acta Chir Scand 1977;143:53-6.

7. Muller C. Recurrent peptic ulcer after proximal gastric vagot­omy. In: Vagotomy in modern surgical practice. London: But­terworths, 1982;312-8.

8. Hollinshead JW, Smith RC, Gillett DJ. Parietal cell vagotomy:experience with 114 patients with prepyloric or duodenal ulcer.World J Surg 1982;6:596-602.

9. De Miguel J. Late results of proximal gastric vagotomy withoutdrainage for duodenal ulcer: 5-9 year follow-up. Br J Surg1982;69:7-10.

10. Jensen H-E, Kjaergaard J, Meisner S. Ulcer recurrence two totwelve years after parietal cell vagotomy for duodenal ulcer.

VOLUME 33, NO.6, 1987

Surgery 1983;94:802-6.11. Gorey TF, Lennon F, Heffernan SJ. Highly selective vagotomy

in duodenal ulceration and its complications. Ann Surg1984;200:181-4.

12. Donahue, PE, Tsai H-S, Yoshida J, Nyhus LM. Proximalgastric vagotomy-the first 25 years. Surg Ann 1985;19:139-73.

13. Donahue PE, Yoshida J, Bombeck CT, Nyhus LM. The endo­scopic Congo red test during proximal gastric vagotomy. Am JSurg 1987;153:249-55.

14. Ornsholt J, Amdrup E, Andersen D, Hostrup H. Arhus countyvagotomy trial: gastric secretory alterations during first yearafter selective gastric and parietal cell vagotomy. Scand JGastroenteroI1983;18:455-63.

15. Moreno Gonzalez E, Narbona Arnau B, Charlo Dupont T,Figueroa Andolla J. Proximal gastric vagotomy. Acta ChirScand 1983;149:69-76.

16. Reid DA, Bird NC, Stoddard CJ, Eyre-Brook I, Johnson AG.Controlled trial of the Grassi (pH) intraoperative test for com­pletion of proximal gastric vagotomy. Surg Gynecol Obstet1984;158:370-374.

17. Hallenbeck GA, Gleysteen JJ, Aldrete JS, Slaughter RL. Prox­imal gastric vagotomy: effects of two operative techniques onclinical and gastric secretory results. Ann Surg 1976;184:435­442.

431