Surg Today Jpn J Surg (1997) 27:247-250

© Springer-Verlag 1997

SURGERYTODAY

Duodenogastric Reflux After Choledochoduodenostomy WASIF ALI, 1 DEEPAK K. AGARWAL, 2 SADIQ S. SIKORA, 1 BHAGWANT R. MITTAL, 3 NARENDRA KRISHNANI, 4

MD. IBRARULLAH, 1 RAMESH K. GUPTA, 4 and SATYENDRA P. KAUSHIK 1

Departments of 1 Surgical Gastroenterology, -' Gastroenterology, 3 Nuclear Medicine, and 4 Pathology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Rae Bareli, Lucknow 226014, India

Abstract: Duodenogastric reflux (DGR) has been implicated in several disease processes. The present study was carried out to document the incidence and evaluate the clinical signifi- cance of D G R after choledochoduodenostomy (CDD). A total of 13 patients who had undergone cholecystectomy with a standard side-to-side CDD for choledocholithiasis or chronic pancreatitis were studied by symptom evaluation, scintigraphy, endoscopy, and gastric mucosal histology at least 6 months after surgery. The scintigraphic findings were then compared with those of 10 patients who had undergone cholecystectomy alone. Only two patients (15%) had mild dyspeptic symptoms. The incidence of DGR after CDD was 69% compared to 20% in the cholecystectomy alone group ( P < 0.05). In the majority of patients the DGR was only mild to moderate and the severity correlated well with the degree of endoscopic gastritis, but not with the clinical symptoms or histological findings. These results indicate that while CDD is associated with a high incidence of DGR, its occurrence does not produce significant clinical symptoms.

Key Words: choledochoduodenostomy, duodenogastric reflux, alkaline reflux gastritis

Introduction

Duodenogastric reflux (DGR) may occur as a natural phenomenon in healthy individuals during the early morning hours or in the postprandial period/,~ How- ever, excessive DGR has been implicated in the gene- sis of dyspeptic symptoms, antral gastritis, alkaline esophagitis, gastric ulceration, intestinalization of the gastric mucosa, and gastric and esophageal carcinoma. 3 Although severe and pathological DGR has mainly

Reprint requests to: S.S. Sikora (Received for publication on Nov. 6, 1995; accepted on July 4, 1996)

been described after alteration or bypass of the pyloric sphincter, +~7 it can also occur in patients with an intact pylorus such as those with cholelithiasis or after cholecystectomy and choledochoduodenostomy (CDD) 2,3,8-16 Nevertheless, few studies have been conducted evaluating the incidence and severity of DGR and its clinical significance after CDD. The present study was undertaken to evaluate the symptoms and incidence of DGR after CDD by scintigraphy. These results were then correlated with the endoscopic and histologic findings.

Materials and Methods

A total of 13 patients, being 6 men and 7 women ranging in age from 23 to 60 years, with a mean age of 36.1 years, who had undergone cholecystectomy and standard side-to-side CDD for choledocholithiasis (n = 12) or chronic pancreatitis (n = 1) were included in this study. A minimum period of 6 months had elapsed after the surgical procedure. None of the patients were on any medication or alcohol and none had undergone any other upper abdominal surgical procedure. All patients were assessed by personal interview, scintigraphy, upper gastrointestingal endoscopy, and histological examination of a gastric mucosal biopsy. Their scintigraphic findings were compared with those of 10 patients who had undergone cholecystectomy alone for symptomatic cholelithiasis acting as a control to the CDD group.

Symptom Scoring

The patients were evaluated by personal interview to assess the symptoms and their severity. The presence and severity of epigastric pain, nausea, and vomiting were scored according to the following scale? 0, symp- toms not present; 1, occasional symptoms; 2, symptoms

248 W. Ali et al.: Duodenogastric Reflux

requiring medical treatment; and 3, symptoms interfer- ing with daily activity. An overall symptom score was obtained for each patient by adding the score of each symptom, with the maximum symptom score being 9.

Scintigraphy

Hepatobiliary scintigraphy was performed using 3-4 mCi of 99mTc parabutyliminodiacetic acid (BULIDA). The anterior abdominal images were taken with a gamma camera (Siemens Digiteac-75 Siemens, Berlin, Germany), each image of 500k counts being taken at 5-rain intervals for 40rain, then for the same count at 1, 2, and 4h. At 60rain, 500 ~tCi of 99mTc sulfur colloid was given orally to localize the stomach. The image interpretation and severity of DGR was assessed and graded according to the following scale: 17 0, no

reflux; 1, reflux only into the antrum; 2, moderate reflux into the body; 3, marked reflux into the body and fundus; and 4, reflux into the esophagus.

Upper Gastrointestinal Endoscopy

Upper gastrointestinal endoscopy was performed in all patients by a single endoscopist (DKA) who was unaware of the symptom score and scintigraphic findings of each patient. The presence and severity of bile pooling, reflux of bile, edema, erythema, friability, and erosions of the gastric mucosa were assessed. Endoscopic gastritis was graded as mild, moderate, or severe based on the severity of the dominant abnormal- ity or abnormalities. 18 Two mucosal biopsy specimens were obtained, one from the antrum and one from the body of the stomach, to look for evidence of reflux gastritis.

Histology

Biopsy specimens were immediately fixed in formal sa- line. Paraffin-processed blocks were sectioned at 3 pm and stained by hematoxylin and eosin. The sections were studied by a single pathologist who had no knowl- edge of the scintigraphic or endoscopic findings, and the histological score was assessed according to the method described by Dixon et al. ~9 A score of 0-3, ranging from normal to severe, respectively, was allotted to each of the following histological features: foveolar hyperplasia, edema and smooth muscle fibers in the lamina propria, and vasodilatation. Acute and chronic inflammatory cells were graded in reverse order to highlight the lack of inflammatory cells in reflux gastritis. Thus, a score of 0 was allotted to a severe increase in acute and chronic inflammatory cells and a maximum score of 6 was assigned to the absence of acute inflammatory cells or the normal/decreased number of chronic inflammatory cells. A combined reflux gastritis score was calculated for each patient, the maximum score being 15. The pres- ence of metaplasia was also looked for.

Statistics

Fisher's exact test was used to compare the frequency of normal and abnormal results in the various groups.

Results

The results of this study are summarized in Table 1. Of the 13 patients, 9 (69%) had varying degrees of DGR after CDD according to hepatobiliary scintigraphy. While 8 of these 9 patients had mild to moderate reflux, as grade 1 in 3 and grade 2 in 5 patients, only 1 had

Table 1. Summary of the results of examinations performed on 13 patients who underwent cholecystectomy with choledochoduodenostomy

Duration Endoscopic Reflux Patient Age after CDD Symptom Scintigraphy gastritis gastritis no. (years) Sex (months) score grade grade score

1 46 M 16 0 3 Moderate 8 2 60 M 15 0 0 Moderate 12 3 28 M 40 0 1 Moderate 8 4 23 F 30 0 0 Mild 11 5 51 M 18 0 2 Moderate 5 6 50 F 39 0 2 Moderate 6 7 45 F 7 0 0 Mild 10 8 50 F 24 1 2 Moderate 5 9 53 F 7 0 2 Moderate 8

10 42 F 22 0 2 Moderate 5 11 40 M 26 0 0 Moderate 8 12 40 M 8 1 1 Mild 10 13 42 F 12 0 1 Mild 9

CDD, choledochoduodenostomy

W. All et al.: Duodenogastric Reflux

I V -

III -

$ c i n t i g r a p h i c II

G r a d e I

0

_ mm

_ mm

• mm mm

mm

Mi ld M o d e r a t e n = 4 n = 9

E n d o s c o p i c Gas t r i t i s

Fig. 1. Relationship between the severity of endoscopic gastritis and duodenogastric reflux (DGR) on scintigraphy (P < 0.05)

249

moderate and severe D G R of grades 2 or 3 on scintigraphy had evidence of moderate endoscopic gastritis. Mild endoscopic gastritis was observed only in patients with grades 0 or 1 D G R on scintigraphy. The severity of endoscopic gastritis correlated with the se- verity of D G R on scintigraphy (P = < 0.05, Fig. 1).

On histological examination, the total reflux gastritis score varied from 5 to 12. None of the patients showed evidence of metaplasia, but Helicobacter pylori were seen in a biopsy specimen from one patient. No correla- tion was found between the severity of histological changes, or the total reflux gastritis score, and the sever- ity of D G R on scintigraphy (Fig. 2). The individual features on histology, considered to be characteristic of bile reflux gastritis - - namely, foveolar hyperplasia, edema and smooth muscle fibers in the lamina propria, vasodilatation, and paucity of acute and chronic inflam- matory cells - - were not significantly correlated with scintigraphic DGR.

severe reflux of grade 3. In the cholecystectomy alone group, mild D G R of grade 1 was observed in 2 (20%) of the 10 patients only. A significant difference was found between the two groups (P < 0.05). Occasional epigas- tric pain with a symptom score of 1 was experienced by 2 (15%) of the 13 patients from the CDD group, both of whom had evidence Of D G R on scintigraphy, of grade 1 and grade 2, respectively. Neither the incidence nor the severity of symptoms correlated with the scientigraphic findings of DGR.

Endoscopy revealed mild gastritis in 1 patient and moderate gastritis in 1 patient, both of whom were symptomatic after CDD. All patients with evidence of

S c i n t i g r a p h i c

G r a d e

I V -

III -

II -

I -

0 -

mmm mm

mm •

• mmm

5 - 9 1 0 - 1 5

n = 9 n = 4

R e f l u x G a s t r i t i s S c o r e ( h i s t o l o g i c a l )

Fig. 2. Relationship betweent the severity of histological changes and DGR on scientigraphy (P = NS)

D i s c u s s i o n

CDD is a procedure of proven clinical merit in the definitive treatment of obstructive lesions of the distal bile duct; however, the incidence of D G R after CDD, as assessed by endoscopy and histology, ranges from 11.5% to 70%, 8,20 22 even though dyspeptic symptoms attributable to D G R have been reported in only 15% of patients. 22 Scintigraphy is also a reliable and sensitive noninvasive method of detecting and quantitating DGR. 3

In the present study, no correlation was found between symptomatology and the presence of D G R on scintigraphy, in accordance with the findings of other studies. ~1,12 Moreover, it has been shown that intragastric bile acid concentration as well as radioiso- topic assessment of the reflux volume are significantly greater in symtomatic patients as compared to asymptomatic patients and controls. 5,6,9-23 These data suggest that it is not only the presence but also the severity of reflux which correlates with the symptoms. The presence of an intact pylorus in patients who have undergone CDD could prevent severe DGR. 4,19,24,25 The fact that severe reflux was uncommon in the present study supports the latter hypothesis and may explain the absence of symptoms in these patients.

Increased D G R after cholecystectomy is due to a loss of bile reservoir, resulting in continuous bile flow into the duodenum? ,12-16 In the present study, the incidence of D G R after cholecystectomy with CDD was found to be significantly greater than that after cholecystectomy alone. A similar observation was made in a recent study by Lujan-Mompean et al., who attributed it to unregu- lated bile flow to the duodenum following bypass of the

250 W. Ali et al.: Duodenogas~ric Reflux

sph inc te r of O d d i and a l t e r ed mot i l i ty of the p y l o r o d u o - d e n u m due to surgical m a n i p u l a t i o n of the d u o d e n u m . 9

The sever i ty of D G R in the p r e s e n t s tudy did no t co r re l a t e with the symptoms , but c o r r e l a t e d well with the endoscop ic findings, con t r a ry to the f indings r e p o r t e d by Ste in et al. 3 H o w e v e r , endoscop ic f indings are sub jec t to i n t e r o b s e r v a t i o n a l va r i a t ions and this might account for such a d i screpancy . A co r r e l a t i on has b e e n shown b e t w e e n the sever i ty of h is to logica l changes and sc in t ig raphy ~7,24-25 in pa t ien t s wi th D G R .

The p re sen t s tudy aga in d id no t s u p p o r t these observa- t ions. This lack of h i s to logica l co r r e l a t i on with the sc in t igraphic sever i ty of D G R has b e e n exp l a ined by Ste in et al. 3 on the basis of fac tors such as the p re sence of H. pylori and /or gastr ic ac id i ty which m a y well a l te r the effect of D G R on the gastr ic mucosa . I t is also poss ib le tha t h is to logica l changes d e p e n d on the gastr ic mucosa l de fense m e c h a n i s m and this w o u l d vary f rom pe r son to person .

In conclus ion, a l though C D D is f r equen t ly assoc ia ted with mi ld to m o d e r a t e D G R , severe D G R is r a re ly seen. Mos t of the pa t i en t s a re a s y m p t o m a t i c and the deg ree of D G R does no t necessa r i ly p r o d u c e s y m p t o m s in all pa t ien ts . M o r e o v e r , whi le pa t i en t s wi th signif icant D G R m a y have m o d e r a t e endoscop i c gastr i t is , his to- logic ev idence of s ignif icant ref lux gastr i t is is no t a lways

found.

References

1. Ritchie AP (1986) Alkaline reflux gastritis: late results on a controlled trial of diagnosis and treatment. Ann Surg 203:537-544

2. Keane FB, Dimagno EP, Malgelada JR (1981) Duodenogastric reflux in humans: its relationship to fasting antroduodenal motility and gastric, pancreatic, and biliary secretion. Gastroen- terology 81:726-731

3. Stein HJ, Smyrk TC, DeMeester TR, Rouse J, Hinder RA (1992) Clinical value of endoscopy and histology in the diagnosis of duodenogastric reflux disease. Surgery 112:796-804

4. Van Heerden JA, Phillips SF, Adson MA, Mcllrath DC (1975) Postoperative reflux gastritis. Am J Surg 129:82-88

5. Ludwig S, Ippoliti A (1979) Objective evaluation of symptomatic bile reflux after antrectomy. Gastroenterology 76:1187-1189

6. Gadacz TR, Zuidema GD (1978) Bile acid composition in pa- tients with and without symptoms of postoperative reflux gastritis. Am J Surg 135:48-52

7. Avgerinos A, Stavropoulos MD, Yalouris A, Rekoumis G, Stavraka-Kakavaki A, Raptis S (1990) Duodenogastric reflux before and after surgical or medical therapy for duodenal ulcer. Am J Gastroenterol 85:150-153

8. Akiyama H, Ikezawa H, Kameya 8, Iwasaki M, Kuroda Y, Takeshita T (1980) Unexpected problems of external choledochoduodenostomy - - Fibrescopic examination in 15 patients. Am J Surg 140:660-665

9. Lujan-Mompean JA, Torralba-Martinez JA, Parrilla-Paricio P, Robles-Campos R, Liron-Ruiz R, Ramirez-Romero P (1994) Quantification of duodenogastric reflux in patients with choledochoduodenostomy. J Am Coll Surg 179:193-196

10. Brown TH, Walton G, Cheadle WG, Larson GM (1989) The alkaline shift in gastric pH after cholecystectomy. Am J Surg 157:58-65

11. Nano M, Palmas F, Giaccone M, Ricci E, Camandona M, Gardino L, Coluccia C, Aloesio R, Fausone G (1990) Bilary reflux after cholecystectomy. Hepatogastroenterology 37:233-234

12. Lujan-Mompean JA, Robles-Campos R, Parrilla-Paricio P, Liron-Ruiz R, Torralba-Martinez JA, Cifuentes-Tebar J (1993) Duodenogastric reflux in patients with biliary lithiasis before and after cholecystectomy. Surg Gynecol Obstet 176:116-118

13. Rees WD, Go VL, Matagelada JR (1979) Simultaneous measure- ment of antroduodenal motility, gastric emptying and duo- denogastric reflux in man. Gut 20:963-970

14. Ehrlein HG (1981) Gastric and duodenal motility in relation to duodenogastric reflux in dogs. Scand J Gastroenterol 16:23-27

15. Brough WA, Taylor TV, Torrance HB (1984) The effect of cholecystectomy on duodenogastric reflux in patients with previ- ous ulcer surgery. Scand J Gastroenterol 19 [Suppl 92]:255-256

16. Svensson JO, Gelin J, Svanvik J (1986) Gallstones, cholecystectomy and duodenogastric reflux of bile acid. Scand J Gastroenterol 21:181-187

17. Thomas WEG, Cooper MJ, McC NJ, Mortensen PA, Burton, Davies ER (1984) The clinical assessment of duodenogastric reflux by scintigraphy and its relation to histological changes in gastric mucosa. Scand J Gastroenterol 19 [Suppl 92]:195-199

18. Tytgat CNJ (1992) Endoscopic gastritis and duodenitis. Endoscopy 24:34-40

19. Dixon MF, O'Connor HJ° Axon ATR, King RFJG, Johnston D (1986) Reflux gastritis: distinct histopathological entity? J Clin Pathol 3:524-530

20. Mittal BR, Ibrarullah Md, Agarwal DK, Maini A, All W, Sikora SS, Das BK, Kaushik SP (1994) Comparative evaluation of scintigraphy and upper gastrointestinal endoscopy for detection of duodenogastric reflux. Ann Nucl Med 8:183-186

21. de Almedia AM, Cruz AG, Aldeia FJ (1984) Side to side choledochoduodenostomy in management of choledocholithiasis and associated disease - - facts and fiction. Am J Surg 147:253- 259

22. Parrilla P, Ramirez P, Bueno FS, Perez Jm, Candel MF, Muelas MS, Robles R (1991) Long term results of choledochoduo- denostomy in the treatment of choledocholithiasis: assessment of 225 cases. Br J Surg 78:470-472

23. Tolin RD, Malmud LS, Stelzer F, Menin R, Makler Jr PJ, Applegate G, Fisher RS (1979) Enterogastric reflux in normal subjects and patients with Billroth II gastroenterostomy - - Measurement of enterogastric reflux. Gastroenterology 77: 1027-1033

24. Ritchie Jr WP (1980) Alkaline reflux gastritis: an objective assess- ment of its diagnosis and treatment. Ann Surg 92:288-298

25. Ritchie WP (1984) Alkaline reflux gastritis: a critical reappraisal. Gut 25:975-987