Surgical selection of infants with gastroesophageal reflux

Surgical

Selection

of Infants

By Dale G. Johnson,

Stephen

With Gastroesophageal

Reflux

G. Jolley, John J. Herbst, and Linda J. Cordell

Salt Lake City, Utah Gastroesophageal

l

debilitating

and

reflux

even

fatal

children.

GER is common

subsides

with

therapy.

time

Operation

cations the

for

that

patient’s

cannot

dietary

treatment

in our decision

in adults.

esophago-

biopsy are useful to document

of reflux

contribute

medical

factors As

effec-

The clinical history

to

important

operation.

presence

seldom

and

be controlled

methods.

scopy and esophageal the

and

and most GER

postural

response

the most

or against

with

produce

is justified only to control compli-

of reflux

remain

can

in infants

in infancy,

or

tively by nonoperative and

(GER)

disease

in older

children,

to the decision

but they

for operation

in

infants. In our hands, gastric scintiscan has provided useful qualitative symptoms

data on reflux-induced

and quantitative

ing. Esophageal

pH monitoring

for reflux evaluation correlations to treatment average

and allows analysis and clinical outcome

or response

in the individual

patient.

A prolonged

of reflux during sleep does appear

to increase the probability ratory symptoms reflux.

Our

patient

selection.

infant

that a patient with respi-

will respond to operative

presently

imprecise

however,

operation

who

does

from

needy

not grow

and for

extubation

the

preemie

attempt

nal feedings

to prevent

flux surgery

is appropriate,

tive. We tive

infants.

who

aspirates

of a process

scarring,

or even respiratory

WORDS:

at every nasojeju-

and cost-effec-

that

chronic illness, persistent

on a

we think antire-

humane,

see no excuse for persisting

management

the

hospitaliza-

long-term

aspiration,

for us to

For

aspirates

prolonged

stunting,

INDEX

not cause

or who

or requires

control of

techniques

must

reflux board, or who requires tion

We have not used

to predict

duration

withhold

empty-

is more quantitative

with reflux patterns.

the reflux patterns

respiratory

data on gastric

with ineffecmay result

in

pain, esophageal

death.

Gastroesophageal

articles were listed for the 5-yr period 19761980. Carre’s classic article’ in 1959 on the natural history of reflux in children documents the fact that symptoms in most refluxing children subside with time and nonoperative treatment. Our experience strongly supports nonoperative management for the majority of children who reflux. Since Carre’s publication, however, the manifestations and long-term consequences of severe reflux have become better understood. We feel there are certain infants whose symptoms and complications are so severe that persistence with nonoperative management is inappropriate and damaging. The proper selection of these infants is the subject of this article. MATERIALS

AND

METHODS

A review of our patients with reflux treated by operation over the past 9 yr revealed that the largest proportion 191) were under

I yr

(I

14 of

of age. These surgical patients were

selected from a very much larger number of patients with reflux symptoms. The numerator

in our surgical fraction of

patients is known to us. The denominator very large for the following reasons: common and occasional regurgitation

is not known but is

( 1) reflux

is extremely

is almost physiologic

in infants; (2) reflux symptoms that interfere with an infant’s well being are treated first and usually with success by the attending prediatrician;

(3) of the poorly responding patients

referred to our gastroenterology

or pediatric surgery services,

over half are managed nonoperatively. Operation

is reserved for patients with on-going complica-

tions of reflux that are not relieved by a rigorous medical trial, usually in the hospital, for 6 wk. Exceptions to the 6-wk

reflux;

esopha-

geal pH monitoring.

trial are patients with advanced esophagitis and stricture or with life-threatening If nonsurgical

respiratory complications.

resolution of reflux

takes place, whether

spontaneously or during medical treatment,

G

ASTROESOPHAGEAL REFLUX (GER) was seldom recognized in North America IO yr ago as a cause of disease or disability in children. Such was not the case in Great Britain and Europe, and reports from abroad concerning treatment by operation were met here with some skepticism and disapproval. The pendulum has now crossed the Atlantic. Reflux has become almost a fad disease in many pediatric centers throughout the United States. The Index Medicus listed 10 North American articles on reflux in children during the 5 yr from 1966 to 1970; 72

Journal of Pediarric Surgery, Vol. 16, No. 4, Suppl. 1 (August), 198 1

it usually occurs

within the first year of life. Our decision, therefore,

to select

some infants

Table

for early operation

is controversial.

1

details the age spread and the sex of our surgical patients under

1 yr. The

male/female

ratio

was

1.7/l.

Table

2

identifies the major indication for operation and the response

From the Departments of Surgery and Pediatrics, Primary Children’s Medical Cenrer and the University of Utah College olMedicine. Salt Lake City, Utah. Address reprint requests to Dale G. Johnson. M.D., Depariment of Surgery. Primary Children’s Medical Center, 320 Tweijth Avenue. Salt Lake City, Utah 84103 0 1981

by Grune

& Stratton,

Inc.

0022-3468/81/1607~010$01.00/0

587

588

JOHNSON

Table

1.

-‘Age and Sex in 114 Infants Selected for Antireflux

Age

Table

3.

Patients

Under

1 yr With

Operation

Surgery

for

ET AL.

GER

Numberof Patients

distribution in months O-2

mo

16

14.0%

Total number of patients

2-4

mo

39

34.0%

Patients with GER only

63

4-6

mo

26

23.0%

Patients with GER and associated conditions

51

6-8

mo

13

11.5%

Types of associated conditions

8-10

mo

8

7.0%

lo-12

mo

12

10.5%

114

(Some patients had more than one) Neurologic

Sex

17

Mental retardation, sewures. Down’s

Males

72

Females

42

syndrome, plegia,

microcephaly,

Pierre-Robm,

spastic

Mobius,

quadri-

hydro-

cephalus

to treatment

among these patients.

were the reason for operation and intractable associated presence

vomiting

disorders,

Respiratory

in 59, failure to thrive in 43,

in 12. Table

many

symptoms

Upper

of which

and the treatment

3 lists the major influence

of the reflux.

associated conditions were present in 5 I of

both

One

I I4

stenosis,

slon. vocal

cord paralysis,

nasopharyngeal

the

sis, phrenic

or more

TEF,

patients.

16

Gl/resplratory

Subglottic

glioma,

nerve

duodenal

pulmonary

hyperten-

cleft

palate,

bronchial

palsy,

stenosis,

steno-

tracheomalacia, esophageal

di-

verticulum Lower

ESOPHAGITIS

AND

STRICTURE

Esophagitis and stricture were seldom seen in our younger patients, although prevention of these late complications is a valid reason for surgical treatment in infants resistant to medical therapy. We have treated advanced reflux strictures in two patients 18 mo of age (Figs. I and 2). Also, one of our premature newborns had severe esophagitis by endoscopy and inflamed periesophageal tissues at operation. The primary reason for operation in this patient, however, was uncontrolled recurrent aspiration, which pre-

Table

7

GI

Malrotatlon.

allergic

forate

Hirschsprung’s

Cardiac ASD,

anus,

enterocolitis.

timper-

5

and thoraclc

coarctation. mitral stenosis, pectus

excavatum Prematurity

14

Multiple anomalies

12

vented weaning from a ventilator. As a rule, severe esophagitis is not the primary complaint in small infants with reflux. although esophagitis may be manifest in the form of extreme irritability.

2 Relief of Svmotoms

NO

Complete

Respiratory symptoms

59

39

6f7”

7

Failure to thnve

43

35

0

8

Vomiting only

12

9

0

3

lnduzatlons

Pamal

None

*Seven deaths from associated conditions: F.E., ASD. pulmonary hypertension. refractory congestive heart failure, respiratory arrest 1 mo postop. N.O.. Reflux corrected. Apneic episodes persisted. Died 1 day following mitral valve replacement for severe Ml. MS..

Reflux corrected. Major reduction m frequency

of recurrent apnea and arrest. Died 1 day following open heart repair of complex CHD. M.J..

Two and a half month premie

treated previously for RDS. recurrent aspiration, RLL collapse. Reflux corrected. Developed pneumothorax and arrest following dilatation of congenital web stenosis of bronchus intermedius. 10 days postop. T.G., Spastic quadroplegic wth seizures and multiple CNS anomalies. Died 1 mo following successful correction of GER. B.H.. PDA,

AV

Down’s

syndrome, corrected duodenal stenosis,

canal. Died 3 mo postop GER correction. M.S..

Subdural hematoma.

seizure disorder. Operation age 5 mo to

control GER. Died 5 mo later-cause?

Fig. treated

1. with

Reflux single

stricture

in

dilatation

and Nissen

18-mo

male.

Successfully

fundoplication.

SURGERY FOR INFANTS WITH REFLUX

589

is 35 of 43 (81%). Among the eight failures had significant associated conditions.

RESPIRATORY

Fig. 2. Reflux stricture in 18-1130female with paraplegia secondary to meningomyelocele. Esophagus split open with attempt at dilatation. Successfully repaired with Thal fundic patch of esophagus, fundoplication, and anterior gastropexy. Stricture resolved with control of reflux. No postop dilatations necessary.

FAILURE

TO THRIVE

Failure to thrive in a refluxing infant is usually associated with persistent vomiting refractory to maximal treatment. In such cases, the failure to thrive is secondary to obvious caloric deprivation because the infant retains and absorbs only a fraction of his intake. Some refluxing infants refuse feedings due to painful swallowing caused by esophagitis. Such caloric deficits, where present, are measurable (through the volume of vomitus) and easily support the decision for surgical correction. In other infants. however, the reason for growth retardation seems to defy quantitation. Reflux is present, and all other studies for metabolic and structural causes for growth failure are negative, and yet the cause-effect relationship between relux and growth lag cannot be proven. Results of antireflux surgery are unpredictable in such cases. With multiple studies to quantitate and characterize the reIIux in problem cases we can improve our accuracy in predicting a good surgical result, but success is far from uniform. Our record for altering the unfavored growth pattern

all

COMPLICATIONS

Infants with respiratory complications of reflux constitute our largest group of patients (59 of 114). Their symptoms include apnea and choking spells, chronic cough, recurrent wheezing, recurrent pulmonary infections, and obvious aspiration pneumonia. The association with reflux is obvious in some cases in which the patient may be observed to reflux gastric content into the pharynx and then choke, cough, turn blue, or suffer respiratory or cardiac arrest. Such positive documentation usually occurs under hospital observation, but occasionally the history of events at home is definitive. More often, however, the temporal relationship in which reflux seems to initiate respiratory symptoms is not at all certain. Both reflux and respiratory symptoms in infants are common; reflux as a cause of respiratory symptoms is much less common. Positive indentification of this causeeffect relationship has posed our greatest challenge in the clinical management of GER.

CLINICAL

STUDIES

Our group has previously published clinical studies involving simultaneous reflux and respiratory monitoring using an indwelling esophageal pH probe and a pneumotachograph.’ The documented sequence of acid reflux (or instillation of dilute hydrochloric acid into the esophagus) followed by choking or apnea is highly suggestive of a causal relationship. Simultaneous recording from upper and lower esophageal pH probes is another approach we have used to increase our confidence that documented reflux and documented respiratory symptoms are cause-effect related. If the lower esophageal probe (Fig. 3) shows abnormal reflux while the upper esophageal probe records a continuous alkaline pH (Fig. 4), it is difficult to implicate reflux in the cause of coincident respiratory symptoms. This type of study, of course, cannot rule out the relationship. It is possible to reAux into the lower esophagus frequently but reflux into the airway very infrequently. Aspiration as infrequent as once per week might be missed by a 24-hr study. Analysis of characteris-

590

JOHNSON

PH 8

7

I HOUR

I

1 SLEEPING

AND SUPINE

PROBE

ET AL

I

AT MID LA

Fig. 3. pH probe in lower esophagus (level of mid-left atrium) recording several episodes of acid reflux with esophageal clearing delayed up to 5 min.

tive certainty surgery.

tics of the esophageal pH study (explained below), in addition to simple frequency of reflux episodes, does increase our accuracy in relating reflux to respiratory disease. When both the lower and upper esophageal probes document acid in the esophagus followed closely by observed coughing, our evidence for a causal relationship is strong, and the probability of total relief following antireflux operation almost certain (Fig. 5). In two patients we have also suctioned acid material from a tracheostomy in sequence with cough and pH probe proven reflux. This type of evidence lends rela-

RADIONUCLIDE

I HOUR

SLEEPING

Fig. 4. pH probe in upper esophagus (just below cricopheryngeus) fails to record any acid reaching the upper esophagus in the same patient (Fig. 3) with frequent lower esophageal reflux.

result

from

reflux

SCAN

The radionuclide scan can also provide proof of the causal relationship between reflux and respiratory symptoms when the test meal can be shown by scan to pass up the esophagus and into the respiratory tract.’ This positive sequence on the scan is picked up infrequently. however, and more often we have to rely on other studies to provide indirect evidence of the causeeetfect association.

PH

6-’

to a good

AND

SUPINE

PROBE

AT T3

I

591

SURGERY FOR INFANTS WITH REFLUX

C.S.I mo.9

The same is true for failure to thrive infants. The good results are dramatic (Fig. 6). Infants severely retarded in growth may not move into a normal weight range, but the change in trend is unequivocal. In 8 of 43 infants, however, the reflux was corrected, but the infants continued to languish. Mental retardation and other anomalies were most often the factors involved and which frustrated our accurate prediction of the postoperative result. FURTHER

STUDIES SELECTION

6

SURGICAL symptoms

PATIENT

SURGERY

Our search for greater accuracy in patient selection for antireflux surgery, particularly with infants, led us to the development of an esophageal pH scoring system. The score is based upon a matrix of data obtained from exophageal pH studies in normal infants and children. The raw

t ,

Fig. 5. A 1-n-10 female with prolonged reflux and delayed clearing of acid from the lower esophagus has documented acid reflux into the upper esophagus immediately followed by observed choking.

Antireflux

FOR

2

DISTAL ESOPHAGUS

tory

TO IMPROVE

surgery

WEIGHT

RESPONSE

in 59 infants

apparently

with

respira-

caused

by reflux and not controlled by medical therapy produced complete relief in 39 of 59 patients. The reflux was controlled by operation in all cases, but 22% continued with at least some of the respiratory complaints, and 12% experienced no improvement. Repeat studies have uncovered initially missed causes for apnea such as seizure disorders, cardiac disease, and tracheomalacia. Some infants have recurrent pulmonary infections with reflux, and they continue to have infections following correction of reflux. The presumed causal relationship is therefore highly questionable.

AGE

(montha)

Fig. 6. Preoperative and postoperative weights connected by a line and superimposed upon the normal weight percentile curves are plotted for 6 patients. Operative control of reflux effects a dramatic improvement in the weight trend even though the severely growth-retarded infants may not approach the normal weight percentile over the 3-mo follow-up period.

592

JOHNSON ET AL.

data with details of the scoring are published elsewhere.4 Our system is an adaptation of the adult score published by Johnson and DeMeester.s In addition to the frequency of reflux, the frequency of reflux greater than 5 min duration. the longest single episode, the percentage of time the esophageal pH was less than four, the state of wakefulness (awake/asleep), and the position of the patient (erect/supine) were factored into the total score. The mean value for the normal patients *2 standard deviations was considered the normal range. We assigned the mean for each variable an arbitrary score of 2 and each standard deviation would add or subtract one point (Fig. 7). Thus, the maximum score for any one parameter is 4, and with 16 variables the theoretical maximum score is 64. In our initial analysis, we were surprised to discover we could not separate normal patients from those with reflux-related symptoms within the first 2 hr after eating. More than 2 hr after eating, however, a clear separation between normal controls and symptomatic refluxers was apparent. All of our normal controls had pH scores less than 58. All of the originally studied symptomatic refluxers had scores in excess of our maximum normal 64 (Fig. 8). We have since identified two patients with reflux stricture and esophagitis with pH scores within normal range. It appears that the stricture may interfere with acid detection higher in the esophagus, but with

l

pe.05

1

2

3

4

5

PH SCORE Fig. 7. Esophageal pH scoring system. For each variable measured in a group of 24 normal children (example. frequency of reflux episodes in 12 hr), the mean value is assigned an arbitrary score of 2. Each SD above or below mean adds or subtracts 1 scoring point. Thus, the maximum normal score for any single variable measured equals the mean + 2 SD or 4. Since we measure 16 variables. our maximum normal pH scow is 64.

p=.OOl 0

400 200

i

i

1 1

;

0 0

IO +hr

t

Post-cibal

~2 hr Post-c&al

Fig. 8. In the first 2 hr following ingestion of a test meal of apple juice (pH 41. the pH score does not separate the patients with clinically symptomatic reflux from the normal asymptomatic controls. Greater than 2 hr after the test meal, the pH score clearly separates the controls (score ~64) from the symptomatic refluxers (score >S4). (Reprinted with permission from Surgery.‘)

this exception the greater than 2 hr postcibal pH score provides a reliable separation between normal and abnormal reflux. The separation between the normal and abnormal reflux in the time period more than 2 hr after eating also stands out when only the frequency of reflux episodes rather than the score is plotted. PATTERNS

0

chltfol

0 Symptomatic

OF

REFLUX

Further analysis of the reflux frequency in the symptomatic patients enabled us to identify two distinct patterns of abnormal reflux, with an additional third pattern that seems to be a combination of the first two (Fig. 9). The type I pattern involves a continuation of the abnormal reflux frequency for more than 3 hr after eating. These patients often have easily demonstrated hiatal hernias, and a high percentage fail at medical therapy and require operation for control of reflux. The type II pattern involves a high frequency of reflux for more than 2 but less than 3 hr after eating. Of great interest is the frequent associa-

SURGERY FOR INFANTS WITH REFLUX

NORMAL Patterns of reflux Fig. 9. according to frequency of reflux episodes/lSmin interval. Following a test meal of apple juice (pH 41, the normal child has e diminishing frequency of reflux for 2 hr. after which reflux essentially ceases. Patients with type I reflux continue with undiminished frequency of reflux episodes beyond 3 hr. Type II patients reflux beyond the normal Z-hr cutoff but do not persist beyond 2.5 hr. Type Ill patients have a diminuation of reflux frequency between 2-3 hr. but abnormal reflux persists beyond 3 hr. (Reproduced by permission of American ./ournal of Surgery.‘)

SYMPTOMATIC

r . In 2.0 -

DURATION

OF

I

SYMPTOMATIC

;l.o:u

1

G

= 0.0

, , , , , , , ,‘, +

2

4

6

g

, , ,I,

, (

IO

14

12

APPLE JUICE POSTCIEAL

tion of increased rather than decreased lower esophageal sphincter pressure, the common association of antropylorospasm, bowel hypermotility manifest as a nonspecific diarrhea, and the common association of respiratory symptoms. The majority of the type II patients will improve with nonsurgical therapy for reflux. Antirefiux surgery in the nonresponders will eliminate reflux in all, respiratory symptoms and pylorospasm in most, and diarrhea in very few. The actual patient details according to symptoms, response, and number of refluxing patients for each pattern type have been published previously.” The type III pattern is a mixture of types I and II, with reflux frequency high at 2 hr, diminishing at 3 hr. but continuing at a high level beyond 4 hr. Many type III patients, like type I, will not respond to a 6-wk trial of medical ,management and will eventually require operation. AVERAGE

TYPE

REFLUX

DURING

SLEEP

A further refinement in our selection of the patient who will respond favorably to antireflux surgery may be obtained by calculating the average duration of reflux during sleep.’ This parameter seems to be a measure of esophageal clearing mechanisms. Logic suggests that abnormal acid clearance with prolonged acid exposure of the esophageal mucosa is also probably corre-

TYPE

m

w

I

I

I

I , I I

I

I 2 4 APiLE JUICE

I

I

6

I

6

I I

I

I

IO

I

I2

I

I I I4

INTERVALS (I5 MINUTES)

lated with the eventual development of esophagitis and stricture, but our data are insufficient to prove this. The patients whose respiratory symptoms resolved after operation (Fig. IO, responders) usually had the average duration of reflux during sleep prolonged beyond the range for the control patients without symptoms. Patients with

30

s

o*-

I

.* *

NO REFLUX

+

IA

.

t

ASYMPTOMATIC CONTROL N.24

RESPONDERS N-9

NON* RES?!3DERS

. RESPIRATORY

SYMPTOMS

*

Fig. 10. The average duration of reflux during sleep (total time esophageal pH < 4 divided by number of reffux episodes) exceeded 4 min (one exception) in patients with respiratory symptoms that were relieved by antireflux surgery. Asymptomatic controls and nonresponding patients had an average duration of reflux less than 4 and usually less than 2 min.

594

JOHNSON ET AL.

persistent respiratory symptoms despite operative control of reflux did not have an increased average duration of reflux preoperatively (Fig. IO, nonresponders). Furthermore, all children with reflux-induced apnea or choking during extended esophageal pH monitoring had a prolonged average duration of reflux.

Table 4. Antireflux Operations According to Reflux Patterns Patternsof GER

EATEF

SURGERY

AND

l/l

1 (9%)

4/35

O/2 2/8 125%)

(11%)

tracheoesophageal The

proportion

for each

flstula of patients

surgery

according

requwing

antireflux

to

reflux

surgery

IS

pattern.

REFLUX

The validity of the reflux pattern analysis is supported by a group of patients we have studied who had previous repair of esophageal atresia and tracheoesophageal fistula (EATEF) as newborns.’ This population was selected because of their known high incidence of symptomatic reflux, which is probably related to a congenital esophageal motility disorder plus surgical alteration of esophageal and gastroesophageal anatomy. We had assumed beforehand that ity of EATEF patients, because of and structural abnormalities of the from birth, would all have abnormal

(50%)

24158 (4 1%)

III

Antireflux operations in patients wth and without esophageal atresla

slmllar

ATRESIA

214

Non-EATEF

pattern.

ESOPHAGEAL

II

I

the majorfunctional esophagus pH scores.

This was not the case. Only 68% of the EATEF patients had abnormal reflux. Analysis of the reflux patterns placed the majority of the refluxing patients in type II. Only one (l/l I) of the type II patients required operation. and this was for control of respiratory symptoms. A smaller number of EATEF patients had the type I pattern, but 50% (2/4) required operation for relief of symptoms (Table 4). This similarity in clinical correlations within reflux pattern types between the EATEF patients and the refluxing patients without previous esophageal surgery lends some support to the validity of the pattern analysis.

REFERENCES I. Carre

IJ: The natural

history of the partial

thoracic

monitoring of the distal esophagus. A quantitative

stomach (hiatus hernia) in children. Arch Dis Child 34:344

of gastroesophageal

353, 1959

I914

2. Herbst

JJ, Minton

reflux causing respiratory Pediatr 95:763-768. 3. Heyman

SB,

Book LS: Gastroesophageal

distress and apnea in newborns. J

children.

et al: An

7. Jolley SG. Herbst JJ, Johnson DC;. et al: Esophageal pH monitoring during sleep identities children with respira-

phageal reflux and aspiration

JA.

Winter

HS,

in children (milk scan). Radi-

tory symptoms from gastroesophageal logy X0:1501-1506.

4. Jolley. SG, Johnson DC;, Herbst JJ. et al: An assessment of gastroesophageal

reflux in children by extended pH

monitoring of the distal esophagus. Surgery 84: 16-22. LF,

reflux in symptomatic 1979

method for the diagnosis of gastroeso-

S, Kirkpatrick

ology 13 1:479-482,1979

5. Johnson

measure

62:325-332.

6. Jolley SG. Herbst JJ. Johnson DC;. ct al: Patterns of postcibal gastroesophageal Am J Surg 138:946-950.

1979

improved radionuclide

reflux. Am J Gastroenterol

DeMeester

TR:

Twenty-four-hour

1978 pH

reHux. Gastroentero-

1981

8. Jolley SC. Johnson DG, Roberts Cc‘. ct al: Patterns of gastroesophageal esophageal

atresia

reflux

in

children

and distal

Pediatr Surg 15:857-862.

1980

following

tracheoesophageal

repair fistula.

of J