Does retroflexed endoscopic examination of the cardia allow prediction of reflux status?

S.J.M. Kraemer, LD. Hill, R.B. Kozarek, R.W. Aye, C.E. Pope II (Seattle)

Thirty years ago, there were many explanations for the absence of gastroesophageal reflux (GER) in normal individuals. Most papers of that era stated that there was no anotomic evidence for a sphincter at the lower end of the esophagus; therefore other explanations for continence must be sought. Several structures which might prevent reflux (many of which were difficult to verify experimentally) were suggested - a mucosal rosette, a flap valve, or the angle of His.

When manometric evidence for a lower esophageal sphincter was offered by Code and associates [l], all attention was focussed on this newcomer to the collection. As time has gone on it seems unlikely that the lower esophageal sphincter is the only barrier to reflux. The contribution of the diaphragmatic crural fibers has been recognized especially during times of exertion or sudden rises in intra-abdominal pressure [2]. Whether or not there is a flap valve mechanism in addition remains an open question.

In experiments done in cadavers with the stomach left in situ, a barrier to the flow of water from the stomach to the esophagus has been demonstrated [3]. This barrier can be disrupted by manual pressure on the gastric fundus or by freeing the attachments of the lower esophageal area. This suggests that passive mechanisms such as a mechanical valve might play a role in the prevention of GER in life.

It was decided to see if there was a grossly recognizable difference in the appearance of the cardia when viewed from below between control subjects and those with reflux. In a preliminary study to seek such a difference, 12 control subjects without a history of heartburn, regurgitation or other esophageal symptoms were examined endoscopically, and the appearance of the gastric fundus distended with air was recorded on videotape. Eleven patients who were being endoscoped for reflux symptoms were also videotaped and the appearance of the cardia in the two groups was compared.

The majority of control subjects revealed a ridge of tissue which tightly closed around the endoscope. This was scored as grade I (Fig. 1). Occasionally, the orifice seemed to open but closed promptly again. This was termed grade II. The patients with reflux tended to have very minimal ridges, and the lumen to the esophagus often gaped open (grade III, Fig. 2). Especially in the patients with erosive esophagitis, there was often a large hiatal hernia and no ridge surrounding the scope. The esophageal mucosa could occasionally be seen through this open orifice (grade IV, Figs. 3A and 3B).

The videotapes were coded and presented to a panel of five gastroenterologists and surgeons who independently graded each tape. There was an interobserver agreement of 80%. There was never more than a one-grade disparity between different

Figure 1. .Grade I valve. The ridge of tissue seems to grip the endoscope, and there is no space around the scope.

Figure 2. .Grade III valve. The normal ridge of tissue is absent and the esophageal lumen is intermittently visible.

Figure 3A. .Grade IV valve. The crural impression defining a hiatal hernia is easily seen, and the endoscope seems to disappear into the fundal sac.

Figure 3B. .Grade IV valve. This is the same patient, only the endoscope has been pulled up so that the entrance into the esophageal lumen can be seen. Note that there is a wide gap between the endoscope and the wall which allows the esophageal mucosa to be seen from below.

observers. The greatest difficulty was experienced in separating grade I from grade II. In the initial group of control subjects, seven had grade I and five had grade II appearances. It was decided to consider either a grade I or a grade II appearance as

Table 1..

	Patient no.	Clinical diagnosis	Esophagitis	pH reflux	LESP	Valve grade
	1.	GERD	+	+	32	IV
	2.	GERD	+	+	17	III
	3.	GERD	+	+	18	IV
	4.	GERD	-	+	12	IV
	5.	Dysphagia	+			III
	6.	Bleeding	+			IV
	7.	GERD	+	+	12	IV
	8.	UGI Bleed	+	+		IV
	9.	GERD	-	+		II
	10.	GERD	+	+	18	IV
	11.	Dysphagia	+			IV
	12.	Barrett's	+			II
	13.	Scleroderma	+			III
	14.	Stricture	+	+	11	IV
	15.	GERD	+			IV
	16.	GERD	+	+	10	IV
	17.	Barrett's	+			IV
	18.	GERD	+			III
	19.	Barrett's	+	+	0	IV
	20.	Barrett's	+			IV
	21.	GERD	+			III
	22.	Barrett's	+	+		IV
	23.	Barrett's	+	+	10	IV
	24.	Dysphagia	+			IV
	25.	Pain	+			III
	26.	GERD	+			IV
	27.	Barrett's	+			III
	28.	GERD	+			IV
	29.	GERD	+			IV
	30.	GERD	+			III
	31.	GERD	-	+	0	IV
	32.	GERD	+	+	0	IV
	33.	GERD	+	+	0	IV
	34.	GERD	+	+	0	IV
	35.	GERD	+	+	50	IV
	36.	GERD	+	_		IV
	37.	GERD	+	+	8	IV
	38.	GERD	+	-		IV
	39.	GERD	+	-		IV
	40.	GERD	+	+	20	IV
	41.	GERD	+	+	22	IV
	42.	GERD	+	+	22	IV
	43.	GERD	+	+	13	IV
	44.	GERD	+	+	17	IV

a "nonreflux" appearance and a grade III or IV was considered to suggest reflux.

Next a prospective study was designed and executed. The definition of a control subject for this study required no esophageal symptoms and a normal 24-h pH monitor value. The reflux group consisted of 44 patients with symptoms of esophageal reflux and either endoscopic appearance of reflux changes or short-term (SART) pH values in the abnormal range. The retroflexed appearance of the gastroesophageal junction was graded by one of three experienced endoscopists who had viewed the original tapes. A summary of the reflux patients is given in Table 1.

If grades I and II are considered normal and grades III and IV considered to suggest reflux, a 2 x 2 table shown in Table 2 can be constructed. The sensitivity and specificity of an abnormal cardia in predicting reflux was 91%. The positive predictive value was 95% and the negative predictive value was 87%.

How did the lower esophageal sphincter pressure fare as a predictor of reflux? Figure 4 shows lower esophageal sphincter pressure (LESP) as a function of both endoscopic grade and reflux status. It can be seen that in the population studied, LESP is a relatively poor predictor of reflux status unless the value is below 10 mmHg. High values of LESP do not mean that reflux is not present.

Table 2..

		Grades III-IV	Grades I-II
	Reflux +	42	2
	Reflux -	2	20

Figure 4. .Endoscopic grade and lower esophageal sphincter pressure (LESP) in controls and patients with reflux. Note that the endoscopic grade separates control subjects and reflux patients almost completely. LESP does not separate the two groups.

Discussion

The advent of flexible endoscopes has allowed inspection of the esophagogastric junction from the gastric side. The appearance of the normal gastroesophageal junction has been well-described by Boyce [4], His description tallies very well with our observations. He also describes the appearance of a hiatal hernia as seen from the gastric side and comments on how tightly or loosely the tissues were applied to the endoscope.

The observations we have made by first examining some control subjects and some patients with esophageal reflux, developing criteria for normality and abnormality, and then prospectively applying these criteria to more control subjects and patients with reflux suggest that such observations may serve a useful clinical purpose. The sensitivity and specificity in this group of subjects and patients is very high, and of a great deal more value in the prediction of reflux status than was the measurement of lower esophageal sphincter pressure in the same individuals. Subsequent experience of several of the investigators in their endoscopic suites has led us to believe that similar studies would produce the same good correlation between endoscopic appearance and the presence or absence of reflux.

The actual physical structures which go into the creation of the gastric fold which surrounds the endoscope are not certain. Direct observation of the gastroesophageal junction through a previously created PEG tract shows that the cardia appears like a closed slit which is very difficult to find until water issues forth from it. In one sense the tissue ridge seen in the retroflexed position is a creation of the endoscope. Yet this appearance is very useful in the prediction of reflux. It is of interest that in 32 patients who were studied after antireflux surgery, the ridge was present whereas it had been absent preoperatively.

We hope that these simple observations, which can be easily made during any endoscopy without unduly prolonging the period of observation, will be of benefit in the evaluation of our patients both preoperatively and postoperatively.

References

1. Fyke FE, Code CF, Schlegel JF. The gastroesophageal sphincter in healthy human beings. Gastroenterologia 1956;86: 135-150.

2. Mittal RK, Fisher M, McCallum RW, Rochester DF, Dent J, Sluss J. Human lower esophageal sphincter pressure response to increased intra-abdominal pressure. Am J Physiol 1990;258:G624-G630.

3. Thor KB, Hill LD, Mercer CD, Kozarek RD. Reappraisal of the flap valve mechanism in the gastroesophageal junction. A study of a new valvuloplasty procedure in cadavers. Acta Chir Scand 1987; 153:25-28.

4. Boyce HW. Hiatal hernia and peptic disease of the esophagus. In: Sivak MV Jr (ed) Gastroenterologic Endoscopy. Philadelphia: WB Saunders, 1987:401-418.