Bile reflux and the Roux en Y anastomosis

Br. J. Surg. Vol. 70 (1983) 393-397
Printed in Great Britain
Proffered review
R. EARLAM
The London Hospital. Whitechapel, London E l .
Bile reflux and the Roux en Y
anastomosis
Bile reflux mto the stomach and then subsequently into the
oesophagus occurs frequently after the two basic forms of
partial gastrectomy Billroth I and Billroth II. Similarly bile
reflux follows the different operations performed to compensate for the temporary slowing of gastric emptying after a
vagotomy—Hemeke-Mikulicz pyloroplasty, Finney pyloroplasty and gastrojejunoslomy. When large amounts of bile enter
the stomach, after a Billroth II partial gastrectomy for
example, bilious vomiting occurs. In the early days of gastric
surgery there were several attempts at altering the techniques of
the original partial gastrectomy to reduce bile reflux, but
another method was to divert bile away from the stomach by a
Roux en Y anastomosis (Fig. 1), an end-to-side jejunojejunostomy, which was successful for gross bile vomiting.
The reflux of smaller amounts of bile either into the intact
stomach or after different types of pyloroplasty or vagotomy
without actual bilious vomiting, can cause symptoms which
arise from the stomach or the lower oesophagus. The different
techniques available for recognition of this duodenogastric
reflux will be discussed. It will then be clear that bile reflux
occurs more frequently than has been previously thought and
that bilious vomiting represents the most extreme form of
reflux, with many other symptoms of lesser amounts of reflux
being unrecognized. Not all patients with bile reflux have
symptoms, even though there may be histological changes in
the mucosa of the stomach and oesophagus. On the other hand
there are some patients who have a very sensitive lower
oesophageal mucosa with minimal histological changes, in
whom all bile must be removed from the stomach before they
lose their symptoms.
Most patients with gastro-oesophageal reflux disease can be
treated by simply repairing the anatomical defect of a hiatus
hernia. Over 80 per cent of the patients do well. Other
operations are based on the reduction of gastric acid, and many
patients can be successfully treated by an antrectomy with or
without the different types of vagotomy. However, in every
surgeon's series there are a few problem patients, and it is these
who may have bile reflux. It is not known whether they can be
identified at the time of their first operation or even whether it
would be essential to do so. The author puts great weight on the
clinical estimation of bile regurgitation by asking the patient
whether fluid comes back into the mouth that is 'yellow, green
or bile-stained'. The surgical treatment of these particular
problem patients is by the Roux en Y procedure.
Apart from reconstruction after a total gastrectomy the
decision to do a Roux en Y anastomosis must not be taken
lightly. Although some surgeons do it as a primary procedure,
in the author's opinion, it is best reserved for failures after an
original procedure for reflux disease, ft not only prevents bile
reaching the lower oesophagus but also reduces gastric acidity
because a vagotomy and antrectomy are done as essential
components in addition to the jejunojejunostomy. Subsequent
complications consist of those that can normally follow a
partial gastrectomy and those that may occur after operations
on the small bowel. They are more frequent than after a partial
gaslrectomy alone and are many more than after a hiatus
hernia repair or a vagotomy and drainage procedure. A
vagotomy is usually added to avoid the complication of stomal
ulceration. Diarrhoea can occur after both a Billroth II
operation and a Roux en Y anastomosis. Some surgeons
consider that a more important factor than the type of
vagotomy is the size of the gastric exit or pyloroplasty. It must
be emphasized that it is not gastro-oesophageal reflux that is
altered, but the corrosive nature of the gastric fluid.
1897
Fig. 1. Roux en Y anastomosis.
This review is concerned with the application of the Roux en
Y anastomosis for the relief of oesophageal symptoms. Emphasis is placed on the physiology and pathology of bile reflux.
No technical or surgical details about the operation are
included, other than the fact that the anastomosis must be at
least 40cm away from the lower oesophagus.
Historical aspects of early gastric surgery relating to bile
reflux
The Roux en Y anastomosis (Fig. 1) was described by Roux in
1897 (1). Cesar Roux was born in Switzerland in Mont-La-Ville
in 1857 and died in 1915. He obtained an MD from Berne and
became professor of surgery, pathology and gynaecology in
Lausanne. Being Swiss French he wrote in French and the
correct name for the anastomosis is Roux en Y grecque. His
other original operation was the Roux loop (Fig. 2), described
in 1907, done to bridge the gap between the oesophagus and the
duodenum (2, 3) after a total gastrectomy. This loop is a
segment of jejunum with its vascular pedicle and should not be
confused with the Roux en Y anastomosis.
The Roux en Y operation was done for postoperative bile
vomiting of such an extreme nature that it could cause death.
Nowadays it is performed for minor degrees of bile reflux
causing less severe symptoms. Nevertheless many lessons were
learnt in the last century which should not be forgotten. It is
impossible to understand the full implications now or in those
early days without knowing about the first gastric operations.
Billroth did his first partial gastrectomy for pyloric cancer in
1881. This was not the original operation because it had been
done experimentally before in dogs, and both Pean and
Rydgier had operated on patients who had died soon afterwards, but Billroth's patient was the first to survive.
In the same year the first gastrojejunostomy was done in
Billroth's clinic by Wolfler as a palliative procedure for another
pyloric carcinoma. In 1884 gastroenterostomy was taken a step
further with the removal of the pyloric tumour and closure of
R. Earlam
394
1907
Fig. 2.
Roux loop.
ihe duodenum to give the Billroth II type of partial gastrectoiny. Originally these operations were done for cancers of the
stomach, but Rydgier's first partial gastrectomy was done for a
gastric ulcer. Hemeke and Mikulicz both performed their
eponymous pyloroplasty independently of each other in 1886.
These were exciting days, because all the classic operations
were done for the first time within 6 years.
At the turn of the century duodenal ulceration became more
common, and the original operations were then applied in such
an enthusiastic fashion that William Mayo could report 307
gastroenterostomies by 1905. The rationale of doing a partial
gastrectomy instead of a drainage procedure was originally
based on removing as much stomach as possible to reduce acid
production. In 1905 Edkins demonstrated that the antrum was
the source of the hormone gastrin, which increased gastric
secretion. Thereafter antrectomies could be rationalized, but
the surgeons actually had no idea of how clever they were
before 1905.
Historically the next great advance was Lester Dragstedt's
truncal vagotomy in 1943. The effect of the vagus on acid
production had been known at the beginning of the century.
Continued gastric secretion after a vagotomy was interpreted
by Pavlov as failure to cut all the vagal fibres. His obsession
with neural reflexes caused him to miss the whole world of
hormones. Dragstedt, after experience with vagotomy in dogs,
persuaded a surgeon to do a simple truncal section alone on
himself for his duodenal ulcer. Later a drainage operation had
to be done, but this was the start of the vagotomy era.
Variations in the method of vagotomy which have followed are
irrelevant compared with this great advance made by Lester
Dragstedt.
The main technical problem in early gastric surgery was the
mortality rate. In 1884 Rydgier reported 43 partial gastrectomies gleaned from the literature with 28 fatalities. The
mortality from gastrojejunostomy between 1881-1885 was 70
per cent and between 1886-1892 it had decreased to 40 per
cent. The majority of these deaths were due to 'regurgitant
bilious vomiting' or 'circulus vitiosus'. The injurious effect of
bile and pancreatic secretions on the stomach was discovered at
a very early stage. The first Billroth II patient eventually died of
bilious vomiting due to a spur obstruction at the anastomosis
and not due to a recurrence. Surgical techniques for preventing
or relieving bile reflux were soon developed. The majority of
early gastrojejunostomies were performed in an antecolic
fashion on to the anterior wall of the stomach. In 1885, von
Hacker, a pupil of Billroth, first described the retrocolic anastomosis onto the posterior wall of the stomach through the
transverse mesocolon. This procedure, together with shorten-
1893
Fig. 3.
Brciun anastomosis.
ing the afferent loop, first suggested in 1901 by Petersen from
Czerny's clinic, dramatically reduced the number of patients
with bilious vomiting.
An end-to-side jejunojejunostomy is a satisfactory way of
dealing with bile in the stomach after a gastrojejunostomy, with
or without an antrectomy: it was first suggested by Wolfler
who demonstrated its effect in a dog in 1883. Doyen described
it again in 1893, but it was Roux who popularized it after
his description in 1897.
The other operation for preventing bile reflux was the sidcto-side jejunojejunostomy first described by Braun in 1893 (4)
(Fig. 3). It was originally applied to the jejunum after a
gastrojejunostomy, when bilious vomiting had to be avoided or
relieved. Its main use nowadays is to prevent bile reflux into the
oesophagus after a total gastrectomy and oesophagojejunostomy. A further modification has recently been described in
which two side-to-side anastomoses are made (5).
Bile reflux in the intact stomach
It is still not proven whether some bile can reflux in normal
asymptomatic people and can therefore be regarded as within
normal limits. Intubation certainly induces nausea and bile
regurgitation, but non-invasive techniques do not have this
disadvantage. Beaumont, the Canadian doctor who looked
after Alexis St. Martin with a gastric fistula, is always cited as
the first to describe bile reflux in a 'normal' person (6). But if
one reads the book in detail, his patient does not appear
entirely normal remembering that he had a large gastric fistula
and was very irascible. The etymological derivation of the word
choleric shows that the ancient Greeks were perfectly aware of
the association between bile and anger.
Bile reflux was first associated clinically and experimentally
with gastric ulceration in 1914 (7, 8) and this association has
been observed on many subsequent occasions (9-15). There is
a definite anatomical abnormality of the pyloric muscle (16)
which probably explains why the reflux persists after the ulcer
heals (17).
Bile reflux also occurs in duodenal ulceration (18, 19). In
pentagastrin studies bile has been found in either the basal
samples or the stimulated juice in the majority of patients (20).
Reflux also occurs in atrophic gastritis (21, 22), alcoholic
gastritis (10), gall bladder dyspepsia (23, 24), chronic nonspecific lung disease (25) and stress ulcers (26, 27).
Bile in the postoperative stomach
The sensitive tests to measure bile reflux into the stomach
developed during the last 15 years have confirmed what was
known at the beginning of the century about bilious vomiting.
Roux en Y anastomosis
They arc important because the results have established that
even a small amount of bile is able to cause symptoms and
gastritis. They help to quantify the degree of pyloric regurgiUition thai can occur postoperatively.
As expected bile reflux is common after a Billroth II type of
partial gastrectomy (13, 27). Over 50 per cent of the resting
juice samples will be bile-stained and 75 per cent of the night
samples (28). Bile is also present after a Billroth I partial
gastrectomy but to a lesser extent (27). The fact that bile reflux
is a cause of gastric ulceration, yet the operation commonly
performed for its cure causes even more bile to enter the
stomach must sound illogical. Perhaps the abnormal anatomical arrangements of the smooth muscle of the lesser curve (29),
which arc said to be responsible for gastric ulceration, may be
the most important factor. A Billroth I partial gastrectomy will
remove this abnormal muscle and allow more bile reflux, but
symptoms and the ulcer usually disappear.
Bile reflux can also occur after a vagotomy of any type (19,
27, 30, 31). It must be realized however that reflux also occurs
in duodenal ulceration, the original disease, so all of these
patients may originally have an abnormal pylorus. Highly
selective vagotomy without drainage procedure is associated
with the least bile reflux (18, 32), No studies have shown
whether there is more reflux after a partial gastrectomy when a
vagotomy is added.
Much more reflux of bile occurs after a gastrojejunostomy
than a pyloroplasty (19. 27, 33), and reflux after a gastrojcjunostomy is higher than after excision of both the pylorus
and antrum.
A Roux en Y anastomosis is followed by the least amount of
bile reflux into the stomach (19, 20, 27, 34). The anastomosis
must be at least 40cm and possibly 50cm from the lower
oesophagus (34). When a partial gastrectomy is converted to a
Roux en Y the amount of bile in the stomach is reduced and the
gastritis can be reversed experimentally (14, 35). Side-to-side
jejunojejunostomy is not as effective as a Roux en Y anastomosis in removing bile from the lower oesophagus, as demonstrated by the radioactive technetium HIDA technique (34). A
jejunal loop has been advocated for intractable symptoms
complicating peptic ulcer surgery, but no bile reflux studies
were done to compare its effect with other procedures (36).
Bile in the oesophagus
Bile in the stomach is a prerequisite for bile in the oesophagus
except after total gastrectomy. Most stomachs secrete acid, so
that the bile is mixed with hydrochloric acid. Much confusion
has occurred because of the term 'alkaline oesophagitis', which
has been favoured by surgeons ignoring the true use of the
word alkaline. If pH 7-0 is accepted as the border between acid
and alkali then true alkaline oesophagitis should only be
present with the intact stomach in pernicious anaemia and
atrophic gastritis, and, in the postoperative state, after a total
gastrectomy. Alkaline oesophagitis and heartburn only occur
in pernicious anaemia (37) and after a total gastrectomy.
Experimentally trypsin has been shown to damage oesophageal
mucosa (38). After total gastrectomy most surgeons do not
favour either an oesophagoduodenal anastomosis or an interposing jejunal Roux loop, because of the complication of bile
reflux and oesophagitis. There have been no quantitative
studies using modern techniques of measuring bile after these
two particular operations where the refluxing material is
alkaline and a total gastrectomy has been performed.
On the other hand bile mixed with gastric acid juice to a pH
below 4-0 is corrosive in the oesophagus, as first demonstrated
in 1951 (39) and confirmed on numerous occasions (40-43).
Experimentally it has been shown that the addition of bile to
acid at any given pH level makes it more corrosive to the
oesophageal mucosa (43-45). Moreover, in pain reproduction
tests adding bile to the perfusing acid fluid causes pain at a
lower threshold (45).
Histological changes in the lower oesophagus have never
been shown to correlate well with symptoms. Recently, with the
realization that pyloric regurgitation of bile can occur through
an abnormal pylorus in gastrooesophageal reflux disease
(46-48), studies have been made to combine the appearances in
the stomach mucosa with those in the oesophagus. Gastritis is
frequently present and is associated with abnormal histological
changes in the oesophageal mucosa (49, 50). The presence of
bile in the stomach refluxing through the gastro-oesophageal
sphincter would appear to be the common factor.
Mechanism of mucosal damage by bile
The simplest experiments are performed by placing bile in the
stomach, or stomach in the bile (51). The former always causes
gastritis. The latter can be achieved by putting a strip of gastric
mucosa in the gall bladder—without subsequent change. The
action of pure bile is minimal, but as the pH drops it becomes
more severe (52, 53). The following sequence of events has been
suggested in an excellent article (48). Bile changes the character
of the gastric mucus (54, 55) so that the underlying epithelial
cells are damaged. The gastric mucosal barrier, which is a
physiological concept, is destroyed (56-59). Hydrogen ions
leak in, histamine is released as a non-specific reaction to
damage and more hydrogen ions may be secreted into the
lumen. Over a long term the gastric acid secretion is reduced
because the damage leads to atrophic gastritis and a progressive loss of parietal cells.
An important chronic change in the gastric mucosal cells,
apart from atrophic gastritis, is gastrointestinal metaplasia and
neoplasia. Cancer in the proximal stump of the stomach is
accepted as a long term complication after Billroth II types of
partial gastrectomy. If a Roux en Y diversion of bile reverses
the histological changes in a partial gastrectomy, it would seem
logical that it must be a safer long term procedure than a
Billroth II type of partial gastrectomy in regard to this
particular complication, but there are no long term studies
available, presumably because of the rarity of this particular
operation.
Tests for bile reflux into the stomach or oesophagus
1. Symptoms alone (27).
2. Bile in the gastric aspirate or in the lower oesophagus seen
macroscopically.
3. Measurements of naturally occuring bile pigments (60),
salts (9) or acids (18) in the gastric juice.
4. Radio-opaque contrast material placed in the duodenum
and observed radiologically (Capper's pyloric regurgitation test) (20).
5. Measurement of artificially introduced substances: (a)
C 14 -labelled bile (61); (b) bromsulphalein (62); (c) indocyanin green and phenol red (62-64); (d} lysolecithin (18,
27, 65, 66, 67); (<?) polyethylene glycol (68); (/) technetium-labelled HIDA (34, 69, 70).
6. Mathematical calculation based on sodium concentration
of gastric juice (19, 62, 71).
7. Indirectly by histological examination of gastric mucosa
(72, 73).
8. Physiological profile of pylorus (47, 63, 74-76).
Indications for the Roux en Y anastomosis
1. After a total gastrectomy.
2. If bile reflux occurs after a pyloroplasty.
3. Failed partial gastrectomy (77).
4. Failed hiatus hernia repair.
5. Failed conservative management of a benign peptic stricture in the lower oesophagus (78, 79).
6. Occasionally as a primary procedure for duodenogastric
reflux with or without oesophagitis.
Medical treatment of bile reflux
Complete cessation of smoking is essential. It is known that the
lower oesophageal sphincter is temporarily weakened after a
vagotomy and then returns to normal, but after a partial
gastrectomy it has a permanently reduced pressure (80, 81).
Many drugs alter this pressure, an important one being nicotine
which is known not only to reduce the resting gastro-oesophageal sphincter pressure, but also to increase bile reflux into the
stomach (75, 82-84).
Bed rest as treatment is out of fashion, although proven to be
beneficial (85), but it should be appreciated that pyloric
R. Earlam
396
regurgitation occurs more frequently in the supine position than
sitting up (10). Experiments measuring the pylonc pressure
profile may vary if this factor is not recorded.
Antacids (86), of which aluminium hydroxide is the best (87,
88), can not only neutralize acid but also adsorb bile salts (89).
Cholestyramine is a specific agent for adsorbing bile salts. It
was originally developed for reducing the level of cholesterol in
the blood (90), but it can be used for symptomatic treatment
(91) although not pleasant to take.
Mctoclopramidc promotes gastric emptying and reduces
pyloric regurgitation. Its main effect on bile in the stomach is
probably due to the increased speed of gastric emptying.
Carbeiioxolone stimulates mucus secretion and prolongs the
life of the gastric epithelial cell. It does not reduce pyloric bile
regurgitation, and only prevents damage to the inucosa. An
alginate preparation mixed with carbenoxolone is marketed in
the United Kingdom as Pyrogastrone.
The effect of cholecystectomy on bile reflux
Cholecystectomy is nowadays not done for vague abdominal
symptoms because the results were unreliable. There are
probably no specific symptoms of indigestion associated with
gall bladder pathology (92). One study showed that patients
with flatulent dyspepsia were equally divided as to whether they
had gall bladder disease or not (93). Cholecystectomy is
notoriously unreliable for relieving the symptoms of flatulent
dyspepsia (24, 94), but it can relieve gastro-oesophageal reflux
symptoms (24, 95).
Bile reflux through the pylorus occurs in many patients with
gall bladder disease (23, 24, 96) and usually reverts to normal
after » cholecystectomy. This would fit in with the fact that
patients with a non-functioning gall bladder are less likely to
have gastrooesophageal reflux symptoms before cholecystectomy than those with normal function (92, 97). The gastrooesophageal sphincter pressures do not alter after cholecystectomy (98), but the oesophageal mucosa is certainly less sensitive
to stimulation by acid dripped into it after a cholecystectomy
(95). The cause of the bile reflux into the stomach is unknown.
There may be a reflex spasm of the pyloric muscle or there may
simply be less concentrated bile in the duodenum after cholecystectomy (97). It is therefore likely that there are no changes
in the oesophagus after a cholecystectomy other than recovery
of damage to the epithelium: there is less bile in the stomach
due to less concentrated bile being secreted into the duodenum
and being available to reflux; there may be some abnormality
of the pyloric muscle which reverts to normal after
cholecystectomy.
Conclusions
Bile reflux into the stomach through the pylorus is an important factor in many upper abdominal disorders. If there is
bile in the stomach it may mix with the gastric juices and reflux
into the oesophagus. If it occurs after a total gastrectomy the
effect will be due only to bile and pancreatic secretions (99).
This subject has been reviewed here and emphasis placed on the
different components such as the particular bile salts (100)
which may cause damage.
Originally the Roux en Y anastomosis was used for gross
bilious vomiting after various failed gastric operations such as
Polya partial gastrectomy or gastrojejunostomy. It was rediscovered about 70 years later for the lesser evils of 'alkaline
gastritis' and bile reflux oesophagitis (101, 102). It is usually
performed in conjunction with a partial gastrectomy and
vagotomy. The latter enables less stomach to be removed and it
can in effect be an antrcctomy. After a total gastrectomy the
Roux en Y anastomosis is one of the methods available for
diverting bile and pancreatic secretions away from the lower
oesophagus.
No techniques concerning the anastomosis have been discussed other than emphasis on the fact that bile must be
diverted at least 40cm away from the oesophageal mucosa. The
results are not discussed here because it is difficult to assess
them when the original patient populations vary so much and
there are no controlled trials. In a recent article it was suggested
that a new reliable non-invasive test for bile reflux was needed
(103). Technetium-labelled HIDA might be the ideal substance.
It is emphasized that the success of a Roux en Y procedure
depends on reducing the acid and bile in the stomach and
eliminating pyloric obstruction; reflux into the oesophagus still
occurs but is asymptomatic. It is the only procedure available
to ensure that no bile refluxes into the stomach.
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Paper accepted 2 February 1983.