Carbohydrate
Malabsorption
Followi ng Fruit
Juice
Ingestion
in Young
Children
Jeftrey
S. Hyams,
MD,
Nancy
L. Etienne,
RN,
Alan
M. Leichtner,
MD,
and
Richard
C. Theuer,
PhD
From the Department of Pediatrics, Hartford Hospital, Hartford, Connecticut, University of Connecticut Health Center, Farmington, and Beech-Nut Nutrition Corporation, Fort Washington, Pennsylvania
ABSTRACT. We performed breath hydrogen analyses in 13 healthy children (9 to 36 months ofage) and seven children (14 to 27 months of age) with chronic nonspe-cific diarrhea after they had ingested pear, grape, and apple juices and a 2% sorbitol solution. Excess breath
H2 excretion was found in virtually all study subjects
following the ingestion of either pear juice (with ap-proximately 2% sorbitol content) or the 2% sorbitol so-lution, in approximately 50% of those ingesting apple juice (0.5% sonbitol), and in 25% of those ingesting
grapejuice (no sorbitol) (P < .001, analysis of variance). No differences were noted between the healthy children
and those with chronic nonspecific diarrhea. Forty per-cent of all study subjects in whom excess breath hy-drogen excretion occurred also had diarrhea and ab-dominal cramping. Carbohydrate malabsorption ap-pears to be frequent following the ingestion of common
fruitjuices and in some children may be associated with
nonspecific gastrointestinal symptoms. Pediatrics 1988; 82:64-68; carbohydrate malabsorption, fruit juice.
resolution of their chronic diarrhea when apple juice was removed from their diet. This study did
not define the cause of this carbohydrate malab-sorption nor did it address whether the phenom-enon was limited to apple juice or might involve other juices as well. Different fruit juices often contain high concentrations of glucose, fructose, sucrose, and the sugar alcohol sorbitol. Whether
malabsonption of one or more of these sugars
oc-curs on whether the high osmolality ofthese juices
is important is unclear. Accordingly, we have
per-formed breath H2 testing in healthy young chi!-dren as well as in those with chronic nonspecific diarrhea after they have ingested several differ-ent fruit juices as well as a sorbitol solution.
PATIENTS AND METHODS
Recent observations have suggested a number
of pathogenetic mechanisms for chronic nonspe-cific diarrhea of childhood including abnormal small intestinal motility,”2 food intolerances,3 di-etary fat restriction,4 excessive fluid intake,5 and carbohydrate malabsorption associated with fruit juice intake.6 This latter theory was based on a
study of five children with chronic nonspecific
diarrhea in whom carbohydrate malabsorption
after apple juice intake was confirmed by breath hydrogen testing. All five children had complete
Received for publication June 11, 1987; accepted Sept 15, 1987.
Presented, in part, at the American Gastroenterological As-sociation, Scientific Meeting, Chicago, May 1987.
Reprint requests to (J.S.H.) Division of Pediatric
Gastroen-terology and Nutrition, Hartford Hospital, Hartford, CT
06115.
PEDIATRICS (ISSN 0031 4005). Copyright © 1988 by the
American Academy of Pediatrics.
Seven children ranging in age from 14 to 27 months were considered to have chronic nonspe-cific diarrhea based on at least a 3-month history
Juice Carbohydrat e (g/100 mL) Osmlkg of H20
Fructose Glucose Sucrose Sorbitol
Apple 6.2 2.7 1.2 0.5 638
Grape 7.5 7.1 1,030
Pear 6.4 2.3 0.9 2.0 764
2% sonbitol 2.0 142
* Because sucrose is subject to inversion in fruit products, glucose, fructose, and sucrose
continually change in concentration during storage. Additionally, the concentrations of these sugars may vary in juice preparations depending upon the particular types of fruit that are used.
None ofthe subjects in either group had exposure
to antibiotics for at least 1 month prior to study. After fasting for 12 hours, each child’s breath H2 was analyzed after ad libitum ingestion of a minimum of 150 mL to a maximum of 240 mL of pear juice, apple juice, white grape juice, and a 2% sorbitol solution, respectively, on four differ-ent occasions during a 14-day period. An interval of at least three days was present between breath
tests. Each child ingested the same quantity of all
four test liquids, and there were no significant differences in the mean volume oftest liquids (200
± 10 mL) ingested between the two study groups. The test liquid was at room temperature at the
time of ingestion. Breath samples were obtained
by mask as previously described,7 prior to and at 30-minute intervals following ingestion ofthe test liquid. For each breath test, the baseline fasting breath H2 concentration was less than 10 ppm in all children. An increase in breath H2 concentra-tion of greater than 10 ppm is considered to be diagnostic of carbohydrate malabsorption.8 A!! parents were provided with a form to record whether diarrhea, bloating, or abdominal pain oc-curred during the eight-hour period after admin-istration of the test liquids.
Osmolality of each of the test liquids was
de-termined in our hospital laboratory by standard techniques (Advanced Cryomatic Osmometer, Advanced Instruments, Needham Heights, MA). Measurements of juice osmo!ality performed throughout several week intervals were virtually identical.
Data are expressed as means ± SEM.
Statis-tical significance ofdifferences between mean va!-ues was determined using t tests, analysis of
van-iance, and the Mann-Whitney test. This study was approved by the Institutional Review Committee at Hartford Hospital. Informed written consent was obtained from a parent of each child studied.
RESULTS
The carbohydrate content and osmolality of each fruit juice and the sorbitol solution are
shown in the Table. Grape juice had the greatest
concentrations of fructose (7.5 g/100 mL) and
glu-cose (7.1 g/100 mL), resulting in a high osmolality
(1,030 mosmol/kg of H20). Pear and apple juices contained less of these sugars but additionally had significant amounts of sorbitol (1.7 to 2.0 g/
100 mL and 0.4 to 0.5 g/100 mL respectively).
The results ofthe breath H2 tests following each of the study juices are shown in the Figure. For each specific test juice there was no significant difference in the mean increase in breath H2 be-tween the children with chronic nonspecific diar-rhea and the control children. However, there were significant differences noted between test
juices for both the chronic nonspecific diarrhea
and control groups (P < .001, analysis of
van-ance). In the children with chronic nonspecific
diarrhea, breath H2 excretion was greaten
follow-ing pear juice and the 2% sonbitol solution than
with either apple on grape juice (P < .05).
Addi-tiona!ly, breath H2 excretion was greater
follow-ing apple juice than grape juice (P < .05). In the
control group, breath H2 excretion was greater
fol-lowing pear juice, apple juice, and the 2% sorbitol
solution than with grape juice (P < .05). Breath H2 excretion was greater following peanjuice than apple juice (P < .05) in these children as well.
Gastrointestinal symptoms developed in
ap-proximately 40% of all children who had an
in-crease in breath H2 excretion following ingestion of either pear juice, apple juice, or the sorbitol
solution. Only two control children had loose
stools following the grape juice. There was no
con-relation between the absolute increase or timing
of breath H2 excretion and the development of
symptoms. An increase in breath H2 was seen as
early as 30 minutes and as late as 90 minutes
following ingestion of the test liquids.
Elimination of fruit juice intake from the diets
of the seven children with chronic nonspecific diarrhea resulted in complete cessation of diar-rhea in three, all of whom had demonstrated in-creased breath H2 following the ingestion of apple
and pear juices and the sorbito! solution. The
MEAN ± SEM E 0. 0. -csJ 100 I I 90 I-< 80
w
70 60w
50 Cl) 40 < 30 2O 10 0 0 A 0 L7±2 6±2 54±10 70±15 34±5 41±13
. 0 1 0 t 0 21±6 15±3 . 0
COlT CN$0 CUT CN$1 COlT CNSD COlT Clii
APPLE GRAPE PEAR SORBITOL
Figure. Maximum increase in breath H2 concentration (parts pen million) over fasting baseline in 13 healthy children (CONT) and seven children with chronic nonspecific diarrhea (CNSD) after ingestion ofapplejuice, grapejuice, pearjuice, and a 2% sorbitol solution. Closed symbols represent children in whom gastrointestinal symptoms (diar-rhea, cramps, bloating) developed following test liquid ingestion. White symbols rep-resent those subjects who remained asymptomatic. No differences noted for each test
solution between CONT and CNSD. For CONT: Breath H2 following pear, apple,
sor-bitol > grape, and pear > apple (P < .05). For CNSD: Breath H2 following pear, sorbitol > apple, grape, and apple > grape (P < .05).
1401
A #{149}
., t 8 A
U A 0
0
8
. 0.
. t 0 0
----c&---&----
-000
r., A
DISCUSSION
Carbohydrate which is not completely absorbed by the small intestine passes into the colon where it serves as substrate for bacterial fermentation producing H2 . Because a portion of this H2 is
ab-sorbed and subsequently excreted through the
lungs, measuring breath H2 is a sensitive
tech-nique for detecting carbohydrate malabsorption.9
Results of our study demonstrate that
carbo-hydrate malabsorption is common following the ingestion of several fruit juices in both children with chronic nonspecific diarrhea and those
with-out. As noted previously, there are several sugars
present in these fruit juices including fructose, glucose, sucrose, and the sugar alcohol, sorbitol. Significantly, the least evidence of carbohydrate
malabsorption was present after the ingestion of
grape juice, despite its having the greatest amounts of fructose and glucose as well as having the highest osmolality. The other test liquids, all of which contain sorbitol, were associated with higher breath H2 excretion, and this was
partic-ularly impressive with pear juice and the 2% son-bitol solution. Previous studies have shown evi-dence of carbohydrate malabsorption by breath H2 analysis following the ingestion of small amounts of sonbitol in both children’#{176} and
adults.” The quantities of apple juice, pear juice,
and the 2% sorbitol solution ingested by our sub-jects would have included from 2 to 5 g of sorbitol.
This may certainly have contributed to the excess breath H2 and development of gastrointestinal
symptoms because sorbito! is only minimally
ab-sorbed by the small intestine. It is important to note that sorbitol is a sugar alcohol naturally oc-curring in many fruits and not commercially added during processing.
An additional contributing factor to the devel-opment of increased breath H2 in some children
may have been the fructose load present in the
fruit juices. Recent reports have suggested that
fructose may be incompletely absorbed by the
small bowel in both children’2 and adults’3”4
in-g of fructose may be associated with an increase in breath H2 in adults.’4 We did not perform breath H2 analysis after the ingestion of fructose alone and, therefore, cannot exclude fructose
ma!-absorption. Nonetheless, it would appear that
fructose malabsorption alone was not a major
fac-ton in most children because few had increased
breath H2 following grape juice which had the greatest concentration of fructose. This apparent effective absorption of the large amount of fruc-tose in grape juice may have resulted from the additional presence of glucose which is known to stimulate fructose uptake in a dose-dependent fashion. ‘
Although not reaching statistical significance in our study groups, the data suggest that greater
breath H2 excretion may follow ingestion of pear
juice (1.7% to 2% sorbitol) than with the 2% son-bitol solution. Recently, it has been suggested that sorbitol and fructose may interfere with each other for absorption.’5 Because pear juice also contains significant amounts of fructose, there may have been an interaction between these two
sugars leading to increased breath H2 excretion.
Despite breath H2 evidence of carbohydrate
malabsorption in virtually all of our subjects
fob-lowing the ingestion of certain juices, only 30% to
40% had gastrointestinal symptoms (carbohy-dnate intolerance). Several factors may explain
this observation. The diarrhea that occurs
follow-ing carbohydrate malabsonption results from the
osmotic effect of the malabsorbed carbohydrate reaching the colon as well as that of the organic acids which are the products of bacterial
fermen-tation of the carbohydrate. Although the human
cobonic mucosa can absorb a large quantity of these fermentation products, there clearly is a sig-nificant intersubject variability in this capac-ity.’6’8 Thus, although ma!absonption of carbo-hydrate as evidenced by breath H2 excretion may occur in many individuals, whether symptoms de-vebop in any may then be influenced by the ability of the individual to handle the cobonic
fermen-tation products resulting from the malabsorption.
Additionally, the development of cramping may
be dependent on the individual’s intrinsic
re-sponse to bowel distention. We observed a poor
correlation between the development of symptoms
and the absolute height of breath H2 excretion.
This observation is similar to that reported
pre-viously in adults.”3
I MPLICATIONS
Our study may have several important impli-cations for the cane of children with both acute
cians traditionally treat acute viral diarrhea with clear liquids, it may be preferable to avoid certain juices. Whether the damaged small intestine
would malabsorb even more carbohydrate than occurred in our study subjects is not known. Sec-ond, it appears that carbohydrate malabsorption following fruit juice ingestion may play a role in the perpetuation of symptoms in some children
with chronic nonspecific diarrhea. Clearly,
addi-tional mechanisms must still be important in
other children with this problem. A brief restric-tion of fruit juices appears to be a simple and
cer-tainly cost-effective diagnostic maneuver in
young children with chronic nonspecific diarrhea. Third, our observations in “healthy” children
sug-gest that gastrointestinal symptoms following the
ingestion of nonexcessive amounts of fruit juices
may develop in them too. These data may help
caretakers avoid unnecessary intervention in
these children when mild nonspecific gastrointes-tinal problems develop.
ACKNOWLEDGMENT
Fruit juices were supplied by the Beech-Nut Nutni-tion Corporation (Fort Washington, PA). Wayne Virk-len performed the specific carbohydrate content anal-yses.
REFERENCES
1. Fenton TR, Harries JT, Milla PJ: Disordered small intes-tinal motility: A rational basis for toddler’s diarrhea. Gut 1983;24:897-903
2. Davidson M, Wasserman R: The irritable colon of child-hood (chronic nonspecific diarrhea syndrome). J Pediatr 1966;69:1027-1038
3. Silverman A, Roy CC: Diarrheal disorder, in Silverman
A, Roy CC (eds): Pediatric Clinical Gastroenterology, ed 3.
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4. Cohen SA, Hendricks KM, Eastham EJ, et al: Chronic non-specific diarrhea: A complication ofdietary fat restriction. Am J Dis Child 1979;133:490-492
5. Greene HL, Ghishan FK: Excessive fluid intake as a cause
of chronic diarrhea in young children. J Pediatr 1983;102:836-840
6. Hyams JS, Leichtner AM: Apple juice: An unappreciated
cause of chronic diarrhea. Am J Dis Child 1985;139:503-505
7. Perman SA, Barr RG, Watkins JB: Sucrose malabsorption
in children: Noninvasive diagnosis by interval breath hy-drogen determination. J Pediatr 1978;93:17-21
8. Barr RG, Watkins JB, Penman JA: Mucosal function and
breath hydrogen excretion: Comparative studies in the clinical evaluation ofchildren with nonspecific abdominal complaints. Pediatrics 1981;68:526-533
9. Levitt MD, Donaldson RM: Use of respiratory hydrogen (H2) excretion to detect carbohydrate malabsorption. J Lab Clin Med 1970;75:937-945
10. Hyams JS: Chronic abdominal pain caused by sorbitol malabsorption. J Pediatr 1982;100:772-773
11. Hyams JS: Sorbitol intolerance: An unappreciated cause
12. Barnes G, McKellan W, Lawrence 5: Detection of fructose
malabsorption by breath hydrogen test in a child with
diarrhea. J Pediatr 1983;103:575-577
13. Ravich WJ, Bayless TM, Thomas M: Fructose: Incomplete
intestinal absorption in humans. Gastroenterology 1983;84:26-29
14. Rumessen JJ, Gudmand-Hoyer E: Absorption capacity of
fructose in healthy adults: Comparison with sucrose and its constituent monosaccharides. Gut 1986;27:1161-1168 15. Rumessen JJ, Gudmand-Hoyer E: Malabsorption of
fruc-tose-sorbitol mixtures: Interactions causing abdominal
distress. Scand J Gastroenterol 1987;22:431-436
16. Bond JH, Curnier BE, Buchwald H, et al: Colonic
conser-vation of malabsorbed carbohydrate. Gastroenterology
1980;78:444-447
17. Stephen AM, Haddad AC, Phillips SF: Passage of carbo-hydrate into the colon: Direct measurements in humans.
Gastroenterology 1983;85:589-595
18. Ruppin H, Bar-Meir 5, Soergel KH, et al: Absorption of short-chain fatty acids by the colon. Gastroenterology
1980;78:1500-1507
CHILDREN WHO START FIRES
While many children occasionally play with fine, those who repeatedly start fires tend to have family trouble, recent studies indicate.
Experts estimate that 60 percent of the arson in large cities is caused by children under the age of 16. In a study, the psychologists Wendy Grolick of
New York University and Robert Cole of the University of Rochester,
ques-tioned 617 children who caused 474 fires in Rochester. Most of them started
fires in innocent ways, playing with matches or looking for objects with lit
matches. They generally showed no signs of drug use or emotional problems.
But a third of those questioned started fires repeatedly or intentionally. Researchers found that these children tended to be angry at someone and neglected or abused at home.
In a separate study, Dr Grolick and Dr Cole questioned 770 Rochester children 6 to 14 years old to determine how common it was for children to play with fire. Ofthose questioned, 38 percent admitted that they had played with fire. The sole factor that distinguished those who played with fine from those who did not was that the fire-players said their parents would “do nothing” if they were caught.
From The New York Times, Dec 17, 1987.
