Carbohydrate Absorption From Fruit Juice in Young Children

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Carbohydrate

Absorption

From

Fruit

Juice

in Young

Children

Melanie M. Smith, MNS, RD; Michael Davis, BS; Fred I. Chasalow, PhD; and Fima Lifshitz, MD

ABSTRACT. Objective. To compare carbohydrate

absorption following ingestion of apple juice and white grape juice in 28 healthy children.

Design. Randomized, double-blind crossover study.

Setting. Outpatient pediatric clinic at Maimonides

Medical Center.

Participants. A total of 18 healthy infants (mean age

6.3 months) and 10 toddlers (mean age 18.0 months),

representing those ages when juice is first introduced (6 months) and when juice comprises a large portion of the diet (18 months).

Methods. Breath hydrogen (H2) testing was

per-formed after age-specific servings of white grape juice or apple juice, 4 and 8 ounces respectively, were consumed. These portions provided approximately 1 g of fructose per kg of body weight. Breath H2 responses of >20 ppm were considered positive, indicating incomplete absorp-tion of fruit juice carbohydrates.

Results. In the combined age groups, carbohydrate

malabsorption occurred more frequently after apple juice consumption (54%) than after white grape juice (19%;

P < .001). Significant differences in area under the breath

H2 curve (AUC) were also found between the two juices in both age groups. Among toddlers, the differences

be-tween the mean peak breath H2 responses were

signifi-cant (48 ppm after apple juice consumption compared with 12 ppm after white grape juice; P < .001). These differences were not significant in the infant group. Significant differences (P < .05) were seen between the

two age groups after consumption of apple juice; the

toddlers exhibited a greater number of positive breath H2

responses and higher peak responses compared with the

infants. Data from the children who drank both juices

showed significant differences in peak breath H2

re-sponses after consumption of apple juice compared with

white grape juice (P < .005).

Conclusions. The study demonstrated less

carbohy-drate malabsorption following ingestion of white grape

juice compared with apple juice in healthy 6- and

18-month-old children. Pediatrics 1995;95:340-344;

carbohy-drate malabsorption, apple juice, white grape juice,

fruc-tose, sorbitol.

ABBREVIATIONS. ppm, parts per million; AUC, area under breath hydrogen curve.

Fruit juice has become a significant part of the

diets of young children. Many factors may be

re-sponsible for this, among them children’s innate

From the Department of Pediatrics, Maimonides Medical Center, Brooklyn, NY.

Received for publication Apr 18, 1994; accepted Nov 21, 1994. Reprint requests to (FL.) Chairman, Department of Pediatrics, Maimonides Medical Center, 4802 Tenth Avenue, Brooklyn, NY 11219.

preference for sweetness, parents’ perception of fruit

juice as a “natural” and “healthful” food, and the

convenience of a juice bottle or box. Unpublished

surveys by juice manufacturers report that about

90% of all infants consume fruit juice by I year of

age. On average, infants drink 5 ounces of juice per

day, but about I % consume more than 20 ounces

daily. Children under 5 years of age average 9

gal-lons of juice per year, of which approximately 50% is

apple juice.

Although all juices contain fructose, the varying

amounts of sucrose, glucose, and sorbitol in different

juices may affect intestinal digestive and absorptive

capacities. For example, one of three healthy adults1

and two of three children2 have been shown to

in-completely absorb 0.7 to 2.0 g/kg body weight of

orally administered fructose. In the presence of

glu-cose, however, the ability to absorb fructose is

en-hanced, especially when equal concentrations of both

sugars are present.3 Fructose in combination with

sorbitol, a hexol that is naturally present in certain

fruits and juices, has been studied in adults and

children.47 In all but one study,4 sorbitol was shown

to intensify the malabsorption of fructose. A review

of the malabsorption of various carbohydrates by

adults and children has been published.8

Investigators have reported carbohydrate

malab-sorption and/or diarrhea in young children

follow-ing the ingestion of various fruit

juices.2’4’9’1#{176}How-ever, studies of carbohydrate absorption in

6-month-old infants have been limited, even though by this

age most children are receiving fruit juices either to

increase dietary variety or as clear fluid

supplemen-tation during episodes of diarrhea. For the average

18-month-old child, fruit juice consumption

contrib-utes substantially to caloric intake. Considering the

significance of fruit juice in the diets of children ages

6 months or 18 months, potential carbohydrate

malabsorption from fruit juice consumption requires

further investigation.

This study evaluated breath H2 excretion in

6-month-old infants and 18-month-old toddlers after

ingesting apple juice and white grape juice. The

se-lection of these juices was based on their

carbohy-drate composition. Apple juice contains more than

twice as much fructose as glucose, and it contains

sorbitol. In contrast, white grape juice contains

ap-proximately equal amounts of fructose and glucose

and no sorbitol. The carbohydrate content and

osmo-lality of these two juices are listed in Table 1. The

results of this study on carbohydrate absorption of

apple juice and white grape juice may influence the

feeding recommendations by pediatricians for

at Viet Nam:AAP Sponsored on September 1, 2020 www.aappublications.org/news

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TABLE 1. Carbohydrate Content* and Osmola1ity of Apple Juice and White Grape Juice

Juice Fructose Glucose Sucrose Sorbitol Osmolality

Apple 6.2 2.7 1.2 0.5 638

White grape 7.5 7.1 1030

*g/loo mL.

1:

mosm/kg H2O.

Modified from Hyams JS, Etienne NL, Leichtner AM, Theuer PC. Carbohydrate malabsorption following fruit juice ingestion in young children. Pediatrics. 1988;82:64-68.

infants and toddlers and the type of juice offered by parents.

Study Design

METHODS

Healthy children, ages 6 months or 18 months, were recruited from the outpatient clinic at Maimonides Medical Center and its affiliated Women, Infants, and Children program. Before their scheduled visit, parents were requested to have the children fast (4 hours for 6-month-old infants and overnight or at least 8 hours for 18-month-old toddlers). Informed consent was obtained from at least one parent of each child. This study was approved by the Institutional Review Board of the Maimonides Medical Center.

A physical examination and review of medical history were performed to exclude children with pre-existing medical prob-lems, abnormal weight gain or growth, antibiotic usage within the previous month, or diarrhea. Also, on the day of the visit, parents were given a diet and health questionnaire regarding dietary intake and fruit juice consumption.

Juice samples were randomly assigned in a double-blind cross-over design. Juices were served at room temperature in 4- and 8-ounce servings for the 6- and I 8-month-old children, respec-tively, typical serving sizes for children of these ages that were designed to provide at least 1 g of fructose per kg of body weight. Failure to consume at least 75% of the specified amount within 15 minutes resulted in the exclusion of two children. No food or beverage other than water was permitted during the testing period.

Breath samples were obtained at baseline and at 30-minute intervals for 2.5 hours. Collected air samples were analyzed for H2 content (QuinTron Instrument Co., Inc., Milwaukee, WI) within 4 to 8 hours of collection. After the testing period, parents recorded the occurrence and severity of symptoms (diarrhea, bloating, gas, abdominal pain). The second juice test was scheduled within 3 to 14 days.

In this study, 28 children completed at least one juice test. The mean ages of the infants and toddlers were 6.3 ‘P 0.5 months and 18.0 ‘t 0.7 months, respectively. All subjects except one infant were drinking fruit juice before the study. Apple juice was the most common juice consumed. Total juice consumption for infants and toddlers averaged 181 4 132 and 438 ‘I’ 215 mL/d, respec-tively. The children demonstrated body weights and lengths be-tween the 10th to 90th percentiles according to age- and gender-specific growth charts and were consuming age-appropriate foods.

Data Analysis

Peak breath H2 response (ppm) was defined as the difference between baseline and the highest breath H2 response. Time to peak breath H2 response (minutes) was defined as the time from beginning of juice ingestion to peak H2 concentration. Integrated breath H2 excretion data were calculated according to Solomons et

al.’1 A peak H2 concentration of 20 ppm was considered

positive.

The breath H2 response data were not normally distributed, thus nonparametric tests were performed. Differences between the means were evaluated using the Mann-Whitney test; correla-tions were calculated with Spearman’s coefficient. Significance was determined at P < .05.

RESULTS

Test juice consumption was similar in each age

group; however, fructose intakes from white grape

juice were slightly greater due to its higher fructose

content (Table 2). All subjects ingested at least 1 g of

fructose per kg body weight except the 6-month-old

infants receiving apple juice who consumed 0.78

g/kg.

The pair-matched data (Fig 1) showed significant

differences in absorption between the two juices for

both infants (P < .01) and toddlers (P < .001). In each

child, apple juice ingestion resulted in greater peak

breath H2 responses compared with white grape

juice. This pattern occurred with normal breath H2

responses (<20 ppm) and positive breath H2

responses (>20 ppm).

The frequency of positive breath H2 responses

among the subjects is shown in Fig 2. In total, 54% of

those who consumed apple juice demonstrated

mal-absorption compared with 19% of those who drank

white grape juice (P < .001). Malabsorption was more

common among toddlers than infants and occurred

more frequently following apple juice ingestion.

Malabsorption following both juices was observed in

one infant and three toddlers.

Significant differences in the absorption of

carbo-hydrates from apple juice and white grape juice were

also seen in the integrated breath H2 excretion (Fig 3).

Both infants and toddlers experienced more

malab-sorption following apple juice (P < .05 and P < .005,

respectively).

Significant differences in mean peak breath H2

re-sponse were seen for the combined age group and

toddlers (Table 3). In the combined age group, the

mean peak breath H2 response after apple juice

con-sumption was 31 ppm compared with I I ppm

fol-lowing white grape juice (P < .001). Infants

demon-strated a mean peak breath H2 response of 20 ppm

(range: 2 to 67 ppm) after apple juice compared with

9 ppm (range: 2 to 31 ppm) following white grape

juice. The mean peak breath H2 response of 48 ppm

(range: 11 to 108 ppm) for toddlers consuming apple

juice was significantly different from the mean peak

response following white grape juice (12 ppm; range:

0 to 42 ppm).

Carbohydrate absorption after apple juice differed

significantly (P < .05) between the two age groups

(Table 3; Fig 2). The toddlers exhibited both a greater

number of positive breath H2 responses and a higher

mean peak breath H2 response compared with the

infants.

TABLE 2. Fructose and Consumption*

Sorbitol Intake Following Test Juice

Apple Juice White Grape Juice Fructose intake, g/kg

6-Month-old infants 0.78 ± 0.10

N=13

1.02 ±0.14 N=12 18-Month-old toddlers 1.00 ± 0.21

N=10

1.31 ±0.23 N=9 Sorbitol intake, g/kg

6-Month-old infants 0.06 ± 0.009

N=13

0 N=12 18-Month-old toddlers 0.08 ± 0.010

N=10

0 N=9

* Mean ± SD.

1:

NS (apple juice versus white grape juice).

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80

Fig 1. Breath H2 responses following consumption of apple juice and white grape juice. S- represents one subject.

Peak breath H2 (ppm)

60

40

NNN:z7

Peak

breath H2 (ppm)

0

120

100

80

60

40

20

0

n=9

Apple White grape

juice juice

P<0.01

Apple White grape

juice juice

P< 0.001

Fig 2. Prevalence of carbohydrate mal-absorption. * P < .001 . Peak breath H2

response > 20 ppm.

-

Apple juice White grape juice

5/13(38)

60

40

20

0

I

1/12(8)

13/23(54)

11 (19)

Both age groups* 6-month-old

infants

18-month-old

toddlers

6-month-old infants 18-month-old toddlers

There was one parental report of gastrointestinal

symptoms following testing with fruit juices. Mild

diarrhea was described in an 18-month-old toddler

who exhibited the highest peak breath H2 response

(108 ppm) after apple juice. Following white grape

juice, she had the highest breath H2 response

(42 ppm) but no symptoms were reported.

DISCUSSION

The results of this study indicate that healthy

6-and 18-month-old children frequently demonstrate

carbohydrate malabsorption following ingestion of

common fruit juices; however, significant differences

in breath H2 excretion were found between apple

juice and white grape juice. In summary, apple juice

was associated with a greater prevalence and

sever-ity of malabsorption than white grape juice in both

age groups and, hence, there must be some factor in

the juice composition leading to differences in the

rates of carbohydrate absorption.

The major carbohydrates present in juice are

fruc-tose, glucose, and sorbitol. Glucose is rapidly

ab-sorbed by an active process; fructose is absorbed by

two separate mechanisms: (1) facilitated transport, a

slow process, and (2) co-transport with glucose, a fast

process. Sorbitol is poorly absorbed by a passive

process.

No. of positive

tests! sample size

(%)

100

80

The carbohydrate composition of apple juice and

white grape juice differ in several aspects, which

may account for the increased malabsorption

follow-ing apple juice. First, there is much more glucose in

white grape juice. This would permit co-transport of

the fructose and reduce the dependence on

facili-tated transport. Second, there is a significant amount

of sorbitol in the apple juice but none in white grape

juice. Both a higher ratio of fructose compared with

glucose and the presence of sorbitol have been

im-plicated as factors that increase fructose

malabsorp-tion.7 In a recent animal study, fructose absorption

was diminished when sucrose was added to equal

amounts of glucose and fructose.12 Interestingly,

when healthy children and adults were challenged

with apple juice and its constituent carbohydrates

(fructose, sorbitol, and a fructose-sorbitol mixture),

the highest breath H2 responses were observed after

consumption of apple juice.4

Some studies have included a few healthy young

children, aged 6 to 18 months, in investigations of

carbohydrate absorption from fruit juices. Our study

differs from these in that all of the children were in

this age range. The findings of this study are

consis-tent with (1) elevated breath H2 responses previously

reported after apple juice ingestion in young children

with chronic nonspecific diarrhea and in limited

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AUG

(ppm. mm

x 100)

_T Fig 3. Integrated breath H2 excretion

following juice consumption. * Mean ±

SE. Comparisons are between apple

juice and white grape juice. t P< .05; P

< .005; § P < .001.

TABLE 3. Peak Breath H2 Response (ppm)*

-

Apple juice

EI

White grape

juice

§ 100

0

.!

6-month-old infants

18-month-old toddlers

Both age

groups

* Mean ± SE.

Comparisons between apple juice and white grape juice: fP = .07 (NS); §P < .001.

Comparison between 6-month-old infants and 18-month-old tod-dlers: #{182}P < .05.

400

Apple Juice White Grape Juice

6-Month-old infants 20 ± 5 N’=13

9 ± 2 N=12 18-Month-old toddlers 48 ± 1091

N=10

12 ± 4 N=9

All subjects 31 ± 6

N=23

11 ± 2 N=21

numbers of healthy controls9”#{176}’13 and (2) lower breath

H2 responses after white grape juice consumption.9

Further, because of the large number and deliberate

division of the study into two discrete age groups,

we showed that there were age-related, significant

changes in carbohydrate malabsorption from fruit

juices.

We feel it is unlikely that the slight differences in

fructose and sorbitol consumption per kilogram of

body weight between the two age groups fully

ac-count for the disparity in breath H2 excretion.

Al-though the larger serving size for the toddlers (8 vs 4

ounces consumed) may have resulted in more rapid

consumption, any potential effect on breath H2

ex-cretion would have been minimized by the

15-minute period allowed for consumption.

Further-more, if there was a developmental lag in fructose

absorption, infants would be expected to display

increased malabsorption. It is possible that large

ha-bitual consumption of apple juice among toddlers

contributes to their increased prevalence and

sever-ity of carbohydrate malabsorption expressed as

breath H2 excretion. In contrast, infants may have a

reduced ability to elicit a breath H2 response. While

exposure of unabsorbed carbohydrates may alter the

type and quantity of colomc bacteria, nonsubstrate

factors, such as colonic pH’4 and gut perfusion,15 also

have been associated with intracolonic gas

produc-tion’6 and may differ according to age.

It is well established that breath H2 responses

cor-relate poorly with symptoms of carbohydrate

intol-erance.17 For example, previous studies have

con-cluded that elevated breath hydrogen response is

present after ingestion by healthy premature infants

of lactose containing formula or human milk.18 In

contrast to milk feedings, which represent the

pri-mary source of nutrition and should be continued in

spite of the breath hydrogen response, juice is

in-tended as a supplemental beverage. In our study,

only one patient reported adverse symptoms

follow-ing the juice tests, despite the high prevalence of

malabsorption. However, parents might not

recog-nize and score carbohydrate intolerance in the young

children.4 Furthermore, in addition to the quantity of

ingested carbohydrate and intestinal absorptive

ca-pacity, the development of symptoms also is

contin-gent upon the rate of gastric emptying, metabolic

activity of colonic bacteria, response of the small

intestine to an osmotic load, and the absorptive

ca-pacity of the colon.19 As these factors may change

with age, increased fruit juice malabsorption with

intolerance may account for the known association

between carbohydrate malabsorption from apple

juice and chronic nonspecific diarrhea of

child-hood.4’8’1#{176}Hence, further studies examining fruit

juice malabsorption, age, and clinical symptoms of

intolerance may be appropriate.

Additionally, we have recently reported that

ex-cess juice consumption may be a contributing factor

in nonorganic failure to thrive.20 These studies

high-light the importance of examining foods and

bever-ages that are commonly recommended for young

children. Thus, when considering appropriate fruit

juices for infants and toddlers, pediatricians should

consider both the carbohydrate content and the

amount of juice consumed.

ACKNOWLEDGMENTS

This study was underwritten by a clinical grant from Welch’s (Concord, MA). Fruit juices were supplied by Welch’s. Additional

support is acknowledged from the Maimonides Research and

Development Foundation.

REFERENCES

1. Ravich WJ, Bayless TM, Thomas M. Fructose: incomplete intestinal absorption in humans. Gastroenterologij. 1983;84:26-29

2. Kneepkens CMF, Vonk RJ, Fernandes J. Incomplete intestinal absorp-tion of fructose. Arch Dis Child. 1984;59:735-738

3. Rumessen JJ, Gudmand-Hoyer E. Absorption capacity of fructose in at Viet Nam:AAP Sponsored on September 1, 2020

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healthy adults: comparison with sucrose and its constituent monosac-charides. Gut. 1986;27:1161-1168

4. Hoekstra JH, van Kempen AA, Kneepkens CM. Apple juice

malabsorption: fructose or sorbitol. IPediatr Gastroenterol Nutr. 1993;16: 39-42

5. Rumessen JJ, Gudmand-Hoyer E. Malabsorption of fructose-sorbitol mixtures: interactions causing abdominal distress. Scand IGastroenterol.

1987;22:431-436

6. Rumessen JJ, Gudmand-Hoyer E. Functional bowel disease: malabsorp-tion and abdominal distress after ingestion of fructose, sorbitol, and fructose-sorbitol mixtures. Gastroenterology. 198895:694-700

7. Nelis GF, Verineeren MAP, Jansen W. Role of fructose-sorbitol malab-sorption in the irritable bowel syndrome. Gastroenterology. 1990;99: 1016-1020

8. Lifshitz F, Ament ME, Kleinman RE, et al. Role of juice carbohydrate malabsorption in chronic nonspecific diarrhea in children. I Pediatr.

1992;120:825-829

9. Hyams JS, Etienne NL, Leichtner AM, Theuer RC. Carbohydrate ma!-absorption following fruit juice ingestion in young children. Pediatrics.

1988;82:64-68

10. Hyams JS, Leichtner AM. Apple juice: an unappreciated cause of chronic diarrhea. Am IDis Child. 1985;139:503-505

I I. Solomons NW, Viteri F, Rosenberg IH. Development of an interval

sampling hydrogen (H2) breath test for carbohydrate malabsorption in

children: evidence for a circadian pattern of H2 concentration. Pediatr Res. 1987;12:816-823

12. Fujisawa I, Riby J, Kretchmer N. Intestinal absorption of fructose in the rat. Gastroenterology. 1991;101:361-367

13. Kneepkens CMF, Jacobs C, Douwes AC. Apple juice, fructose, and chronic nonspecific diarrhea. Eur IPediatr. 1989;148:571-573

14. Perman JA, Modler 5, Olson AC. Role of pH in production of hydrogen from carbohydrates by colonic bacteria! flora: studies in vivo and in vitro. I Clin Invest. 1981;67:643

15. PermanjA, Waters LA, Harrison MR. Yee ES, He!dt G. Breath hydrogen flora reflects canine ischemia. Pediatr Res. 1981;15:1229

16. Barr RG, Woo!dridge JA, Kramer MS. Pless lB. Methane excretion in infants: prevalence and response to formula change. Pediatr Res. 1983; 17:183A

17. Rosado JL, Allen LH, Solomons NW. Milk consumption, symptom response, and lactose digestion in milk intolerance. Am IClin Nutr.

1987;45:1457-1460

18. McLean WC, Fink BB. Lactose malabsorption by premature infants: magnitude and clinical significance. IPediatr. 1980;97:383-388.

19. Lebentha! E, Rossi TM, Nord KS, Branski D. Recurrent abdominal pain and lactose absorption in children. Pediatrics. 1981;67:828-832

20. Smith MM, Lifshitz F. Excess fruit juice consumption as a contributing factor in nonorganic failure to thrive. Pediatrics. 1994;93:438-443

THE VIEW FROM COLUMBIA-PRESBYTERIAN MEDICAL CENTER:

Is This Really the Future?

Emerging as hospitals’ most promising source of new patients are clinics like

Columbia-Presbyterian Eastside, which, in health care jargon, are called “centers,”

lest potential patients confuse these gleaming outposts with conventional clinics

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enclaves, upscale New York neighborhoods, affluent suburban communities, and

even distant American expatriate communities in Eastern Europe.

Four months ago, Columbia-Presbyterian created a satellite in Moscow and more

centers are planned for Warsaw, Prague, St. Petersburg, Budapest, and possibly

Beijing.

“Our feeling is that there will be no hospitals in the future,” said Dr. William T.

Speck, president of Columbia-Presbyterian. “And probably, in the next 10 or 20

years most of the activity will take place in a center or maybe even in homes.”

At Columbia-Presbyterian, the top executives are already mulling over what to

do with the huge Washington Heights hospital as it empties out to the sateffites.

“Hospitals are going to get smaller and smaller and maybe the hospitals might

turn into something else,” Dr. Speck said. “Perhaps a gymnasium or a flower

shop.”

New York Times. January 22, 1995.

Noted by J.F.L., MD

Editor’s Note: Large private Urban teaching hospitals certainly have a rough time ahead.

I’m stunned to think they could vanish. I’m baffled as to how one could teach students or

do clinical research in these new center boutiques.

JFL

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1995;95;340

Pediatrics

Melanie M. Smith, Michael Davis, Fred I. Chasalow and Fima Lifshitz