8
AMERICAN ACADEMY OF PEDIATRICS 240 PEDIATRICS Vol. 62 No. 2 August 1978 Committee on Nutrition The Practical Significance of Lactose Intolerance in Children Lactose intolerance has been reviewed in published statements by the Protein Advisory Group of the United Nations System,’ the Food and Nutrition Board of the National Research Council,2 and the American Academy of Pediat- rics, Committee on Nutrition.’ Each of these statements deals principally with the advisability of encouraging population groups with a high rate of lactose intolerance to consume nutritional- ly beneficial quantities of milk. All three state- ments conclude that it is inappropriate to discour- age the use of milk on the basis of lactose intolerance. Nevertheless, controversy over the practical significance of the widespread preva- lence4’5 of lactose intolerance has continued. DEFINITIONS Lactose intolerance is defined’ as a clinical syndrome of abdominal pain, diarrhea, flatulence, and bloating after the ingestion of a standard lactose tolerance test dose (2 gm of lactose per kilogram of body weight or 50 gm /sq m of body surface area, maximum 50 gm in a 20% water solution). If a maximum increase in blood glucose level of less than 26 mg/dl is observed after a lactose tolerance test dose, lactose malabsorption is diagnosed.’ Lactose intolerance is classified as primary, secondary, or congenital. Lactose intol- erance is classified as primary when it is observed with no history or signs of underlying intestinal disease. If there is gastrointestinal disease, it is usually classified as secondary. Primary and secondary lactose intolerance are not uncommon; however, congenital lactose intolerance is rare. This form is present at birth, the histologic features of the gastrointestinal mucosa are normal, and brush-border lactase activity is low or completely absent.” The three forms of lactose intolerance must be considered separately to avoid confusion. PRIMARY LACTOSE INTOLERANCE Major areas of concern in reviewing the practi- cal implications of primary lactose intolerance are (1) the prevalence at specific ages in particu- lar population groups, (2) the relationship between primary lactose intolerance and intoler- ance to quantities of milk usually consumed, (3) response to hydrolyzed lactose milk, and (4) the absorption of other nutrients in the presence of amounts of lactose that surpass digestive capacity but do not produce symptoms. Studies on Lactose Intolerance The widespread prevalence of lactose malab- sorption and intolerance in children is well docu- mented in a review by Jones and Latham.4 Prevalence at specific ages in a particular popu- lation group varies. In some groups, 90% preva- lence is observed by age 4 years; in others it remains much lower throughout life. Similar information on children of American ethnic groups has been published recently.5’7 Paige and co-workers” studied 1 16 black chil- dren 13 to 59 months old. Twenty-nine percent of these children had lactose malabsorption, and 18% had signs of intolerance. Black children 4 to 9 years old were studied by Garza and Scrimshaw.9 They reported lactose intolerance in 1 1% of those 4 to 5 years old, 50% of those 6 to 7 years old, and 72% of those 8 to 9 years old. Paige and co- workers’#{176} studied another group of children 6 to 13 years old. Fifty-four percent had lactose malabsorption and 65% had symptoms of intoler- ance. Haverberg et al.” and Kwon et al.’2 studied black patients 14 to 19 years old and reported lactose malabsorption prevalence rates of 83% and 81%, respectively. Studies of Mexican-American children have also been reported. Woteki et at.” studied 282 Mexican-American children who were 2 to 14 years old. Eighteen percent of the 2- to 5-year-old children were intolerant to lactose. This preva- lence increased to 56% in the 10- to 14-year-old children. Sowers and Winterfeldt” found a simi- lar prevalence (50%) in 9- to 21-year-old Mexican- by guest on March 18, 2021 www.aappublications.org/news Downloaded from

The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

  • Upload
    others

  • View
    6

  • Download
    0

Embed Size (px)

Citation preview

Page 1: The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

AMERICAN ACADEMY OF PEDIATRICS

240 PEDIATRICS Vol. 62 No. 2 August 1978

Committee on Nutrition

The Practical Significance of Lactose Intolerance inChildren

Lactose intolerance has been reviewed in

published statements by the Protein AdvisoryGroup of the United Nations System,’ the Food

and Nutrition Board of the National Research

Council,2 and the American Academy of Pediat-

rics, Committee on Nutrition.’ Each of these

statements deals principally with the advisability

of encouraging population groups with a high

rate of lactose intolerance to consume nutritional-

ly beneficial quantities of milk. All three state-

ments conclude that it is inappropriate to discour-

age the use of milk on the basis of lactoseintolerance. Nevertheless, controversy over thepractical significance of the widespread preva-

lence4’5 of lactose intolerance has continued.

DEFINITIONS

Lactose intolerance is defined’ as a clinical

syndrome of abdominal pain, diarrhea, flatulence,and bloating after the ingestion of a standard

lactose tolerance test dose (2 gm of lactose perkilogram of body weight or 50 gm /sq m of body

surface area, maximum 50 gm in a 20% water

solution). If a maximum increase in blood glucose

level of less than 26 mg/dl is observed after alactose tolerance test dose, lactose malabsorption

is diagnosed.’ Lactose intolerance is classified as

primary, secondary, or congenital. Lactose intol-

erance is classified as primary when it is observed

with no history or signs of underlying intestinal

disease. If there is gastrointestinal disease, it isusually classified as secondary. Primary andsecondary lactose intolerance are not uncommon;

however, congenital lactose intolerance is rare.

This form is present at birth, the histologic

features of the gastrointestinal mucosa are

normal, and brush-border lactase activity is low

or completely absent.” � The three forms of

lactose intolerance must be considered separatelyto avoid confusion.

PRIMARY LACTOSE INTOLERANCE

Major areas of concern in reviewing the practi-

cal implications of primary lactose intolerance

are (1) the prevalence at specific ages in particu-

lar population groups, (2) the relationship

between primary lactose intolerance and intoler-ance to quantities of milk usually consumed, (3)response to hydrolyzed lactose milk, and (4) the

absorption of other nutrients in the presence of

amounts of lactose that surpass digestive capacitybut do not produce symptoms.

Studies on Lactose Intolerance

The widespread prevalence of lactose malab-

sorption and intolerance in children is well docu-mented in a review by Jones and Latham.4

Prevalence at specific ages in a particular popu-

lation group varies. In some groups, 90% preva-lence is observed by age 4 years; in others itremains much lower throughout life. Similar

information on children of American ethnic

groups has been published recently.5’7Paige and co-workers” studied 1 16 black chil-

dren 13 to 59 months old. Twenty-nine percent ofthese children had lactose malabsorption, and18% had signs of intolerance. Black children 4 to 9

years old were studied by Garza and Scrimshaw.9

They reported lactose intolerance in 1 1% of those

4 to 5 years old, 50% of those 6 to 7 years old, and

72% of those 8 to 9 years old. Paige and co-workers’#{176} studied another group of children 6 to

13 years old. Fifty-four percent had lactosemalabsorption and 65% had symptoms of intoler-

ance. Haverberg et al.” and Kwon et al.’2 studied

black patients 14 to 19 years old and reported

lactose malabsorption prevalence rates of 83%

and 81%, respectively.Studies of Mexican-American children have

also been reported. Woteki et at.” studied 282Mexican-American children who were 2 to 14years old. Eighteen percent of the 2- to 5-year-old

children were intolerant to lactose. This preva-

lence increased to 56% in the 10- to 14-year-old

children. Sowers and Winterfeldt” found a simi-lar prevalence (50%) in 9- to 21-year-old Mexican-

by guest on March 18, 2021www.aappublications.org/newsDownloaded from

Page 2: The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

AMERICAN ACADEMY OF PEDIATRICS 241

American children. In a study of 301 adolescents

and young adults’5 in rural Mexico, 222 of themwere classified as having lactose malabsorption,

but only 86 of these reported symptoms.American Indians have been studied by Casky

and co-workers.” Using hydrogen breath analysis,

lactose malabsorption was found in 20% of 3- to5-year-old children, in 10% of those 6 to 12 yearsold, and in 70% of those 13 to 19 years old.Newcomer et al.’7 reported a similar study inAmerican Indians in which 104 subjects 5 to 17

years old were studied. Lactose malabsorption

was diagnosed in 63% to 74% of the groups

stratified by age (5 to 6 years, 7 to 8 years, and soforth). Symptoms were reported in 76% of the

children with lactose malabsorption. Prevalence

of lactose intolerance at specific ages was not

reported.

Prevalence of lactose malabsorption in whitechildren tends to be much lower than in these

other groups. Persons classified as white in this

country tend to be heterogeneous; therefore, dataare difficult to compare with studies published in

countries with more homogeneous populations.Data presented by Woteki et al.’3 and Garza and

Scrimshaw9 are representative. Lactose intoler-ance is rarely observed in 2- to 6-year-old chil-

dren, and increases to about 30% among adoles-

cents. Lebenthal et al.’8 have reported lactaselevels from 172 of 1,077 biopsy specimens. Thegroups studied were white and were healthy

siblings and parents of patients with cystic fibro-sis, children with failure to thrive without diar-rhea, and patients with “irritable colon syn-

drome.” No low lactase activity was encounteredin children less than 5 years old.

Comparable data on the prevalence of lactoseintolerance in American children from other

ethnic backgrounds who were expected to have a

high prevalence of lactose intolerance (e.g.,

Chinese, Japanese, and Greek) are not available.Assessing the relationship between lactose and

milk consumption is also important in determin-mg the practical significance of lactose intoler-ance in children. Comparison of the standard

lactose tolerance test dose with quantities of milk

normally consumed shows that the test dose isrepresentative of the amount of milk consumed

by young infants but not of that consumed byweaned children. The 200 to 250 ml of milk

usually consumed at one sitting by the latter

children contains 12 gm of lactose. This issubstantially less than the 2 gm/kg usuallyprovided in the lactose tolerance test.

Paige et al.’9 reported that lactose intolerancein elementary school children adversely in-

fluenced their acceptance of moderate amounts

of milk. Milk’s significant role in publicly spon-

sored, supplemental feeding programs led Paige

and other investigators to study lactose intoler-ance further. Paige et al.5 found no differences in

milk consumption between lactose-tolerant and

lactose-intolerant black children 13 to 59 months

old. Garza and Scrimshaw9 found no differences

in milk consumption between lactose-tolerant

and lactose-intolerant black children 6 to 7 and 8

to 9 years old, although the 8- to 9-year-old black

children consumed less milk regardless of lactose

tolerance status than a comparable group ofwhite children. Woteki et al.” reported no differ-

ence in milk consumption by the lactose-tolerant

and lactose-intolerant Mexican-American chil-

dren they studied. In a study in rural Mexico,’5

conflicting results were obtained and do not helpto determine whether lactose malabsorption

interferes with milk consumption.

Stephenson and Latham2 studied slightly older

children with lactose malabsorption; no differ-

ence in milk consumption was observed betweenthe lactose-tolerant and lactose-intolerant sub-

jects in this study. In Newcomer and co-workers’study’7 of American Indians, two thirds of the 156subjects studied were less than 18 years old, andthose with lactose malabsorption had mean daily

lactose intakes of 19 gm compared to 25 gm in

those with lactose absorption. Woteki et al.”

reported no differences in milk intakes betweenthose with lactose absorption and malabsorption,but children classified as Anglo-American drank

more milk than the Mexican-American children.

In contrast, Paige et al.2 ‘ reported that 50% of 6-

to 12-year-old children with lactose malabsorp-

tion consumed less than one-half pint of milk

offered in school feeding programs. They found

that children with lactose malabsorption whowere classified as milk-drinkers had higher

increases in blood glucose level than those classi-fled as non-milk-drinkers. Lebenthal et al.18 havealso reported greater milk consumption (> 960

mi/day) in individuals with high intestinal lactase

levels and their families than in patients and

families with low lactase levels (< 250 mi/day).The question of tolerance to various lactose

intake levels in intolerant subjects and those with

lactose malabsorption has also been examined.Garza and Scrimshaw9 report that, despite thesignificant prevalence of lactose intolerance they

observed in 4- to 9-year-old black children, no

child was intolerant to 240 ml of milk. In contrast,

Mitchell et al.,22 who studied 11- to 18-year-old

black adolescents, found that 21% had symptoms

after consuming 240 ml of milk. In double-blindstudies, Haverberg et al.” and Kwon et al.’2report, respectively, that 28% and 9% of adoles-

by guest on March 18, 2021www.aappublications.org/newsDownloaded from

Page 3: The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

242 LACTOSE INTOLERANCE

cents with lactose malabsorption had symptoms

after drinking 240 ml of milk, as did 16% and 19%

of those with lactose absorption. In a slightly

older age group studied by Stephenson andLatham,2#{176} all those with lactose malabsorption

could tolerate 240 ml of whole milk without anyor only mild symptoms. In studies of nativeAmerican Indians, Newcomer et al.2’ report thatall of the subjects they studied who had malab-

sorption (6 to 62 years old) tolerated amounts oflactose equivalent to 240 to 300 ml of milk taken

with a meal with no intestinal symptoms attribut-

able to lactose. In contrast, lower tolerance levels

are reported in older adults by Bayless et al.24 and

in Peruvian children by Paige et al.25 Studies from

other countries have reported a lack of symptoms

in lactose-intolerant children comparable to those

reported here.2’27

A possible solution for circumventing intoler-ance to normal intakes of milk is to hydrolyze the

lactose. Although studies such as those of Jones et

al.2” report that lactose hydrolysis substantially

increases milk tolerance in adults, other studies

cast doubt on the efficacy of lactose hydrolysis in

children. Paige and co-workers29 tested whole

milk, 50% hydrolyzed lactose milk, and 90% hy-drolyzed lactose milk in 22 black 13- to 19-

year-old subjects with lactose malabsorption.

Three of these teenagers reported symptoms to

untreated whole milk and to 90% hydrolyzedlactose milk. None reported symptoms to 50%hydrolyzed lactose milk. Similarly, Kwon et al.’2reported that 28 of 45 teenagers with lactosemalabsorption did not experience symptoms to

240 ml of whole milk or lactose-free milk. Ten of

the others had inconsistent symptoms; some hadsymptoms to lactose-free milk only, some to both

lactose-free milk and whole milk, and others to240 ml but not 480 ml of whole milk. Seven

subjects had consistent symptoms, but none hadsymptoms to 240 ml of milk, with or withoutlactose.

Milk in the Diet

The importance of milk in the American diet

rests on its high nutrient content. The U.S.Department of Agriculture30 estimates that dairy

products, excluding butter, contribute only 11%

of the available food energy; however, they

provide 75% of the calcium, 39% of the riboflavin,

35% of the phosphorus, 22% of the magnesium,

20% of the vitamin B,2, and substantial propor-

tions of other nutrients. The question of the

bioavailability of these nutrients in the presenceof lactose malabsorption without symptoms ofintolerance is, therefore, important. Unfortunate-

ly, little data are available. Significant malabsorp-

tion is unlikely if there are no symptoms; howev-

er, the chronic effects of subtle differences in

bioavailability of various nutrients might besignificant, especially under conditions of margi-nal intakes. There are substantial data on the

“malabsorption of lactose,” but there are no

studies estimating metabolizable energy inlactose-containing diets of children with lactose

malabsorption. Less increase in blood glucose

levels has been demonstrated2’ in those withlactose malabsorption than in those with lactose

absorption after milk ingestion. The possibilitythat slower but sustained digestion of lactose is

responsible for these smaller increases remains

unknown.

A metabolic study in which milk provided alldietary protein was designed by Calloway andChenoweth” and was conducted in lactose-toler-

ant and -intolerant adults. After adjustments formetabolizable energy were made, no effect onnitrogen balance was demonstrated. Unpublished

results from this study indicate that calcium,phosphorus, and magnesium absorption also were

not influenced by the presence of lactose.Leichter and Tolensky,’2 in a study �n weaned

rats that were fed lactose-containing diets,

obtained suggestive evidence that lactose mayreduce protein and fat absorption in animals with

low lactase activity. Bowie” reported the effectsof lactose-induced diarrhea on nitrogen and fatabsorption. Nitrogen absorption was depressed in

those with lactose malabsorption who were fedmilk compared to a disaccharide-free diet, but

nitrogen retentions were similar with both diets.No differences in fat absorption were noticed. In

a separate study by Bowie et al.,’4 absorption was

studied by using xylose. No difference in xyloseexcretion was observed when malnourished,

lactose-intolerant subjects were fed whole milk or

a disaccharide-free formula. A recent study’5

conducted in 2- to 8-month-old infants comparedcalcium and magnesium absorption when un-treated milk, Iflilk treated with lactase tenminutes before feeding, and a lactose-free milkwere fed. Calcium and magnesium absorption

was best (72% and 81%, respectively) with

lactase-treated milk and poorest (calcium 37%

and magnesium 39%) with lactose-free milk. The

infants were presumably lactose tolerant.

Summary

Lactose intolerance is observed in black andMexican-American children by age 3 years, and itprobably occurs in other non-northern European

ethnic groups at a similar age. However, intoler-

by guest on March 18, 2021www.aappublications.org/newsDownloaded from

Page 4: The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

AMERICAN ACADEMY OF PEDIATRICS 243

ance to the consumption of 250 ml of milk

apparently is rarely seen in preadolescents.

Current research on the response of adolescentsto hydrolyzed lactose milk suggests that the

symptoms observed in lactose-intolerant subjects

after milk ingestion may be unrelated to lactoseor may be mild enough to be of little practical

significance. The effects of undigested lactose onnutrient absorption has received little attention,

but preliminary data suggest that this is not a

problem, except perhaps when overall intakes aremarginally adequate.

SECONDARY LACTOSE INTOLERANCE

The predominant view at present is thatprimary lactose intolerance is genetically prede-

termined. The following observations supportthis view: its prevalence among apparentlyhealthy populations, its absence among specificgroups,36’8 the inevitable decrease with age inlactase activity in most mammalian species,39 andthe apparently noninducible nature of the

enzyme in humans.2’4#{176} However, the environ-

ment’s role in accelerating the age of lactoseintolerance, determining the severity of its

expression, and increasing the prevalence within

population groups has not been assessed. Fewstudies have been directed at a basic understand-

ing of the physiology of the intestinal mucosal

cells as it relates to lactose intolerance and

malabsorption. Yet the importance of the envi-

ronment is repeatedly demonstrated by the

apparently transient decrease in lactase activity

and intolerance to lactose commonly associated

with gastrointestinal disease or significant malnu-

trition. This condition is classified as secondarylactose intolerance. Areas of concern in assessing

its practical implications are (1) its significance in

the treatment of malnutrition, which is common

to gastrointestinal disease; and (2) the “reversibil-

ity” of this condition and its effects on the

expression of a presumably, genetically deter-mined decrease in lactase.

Lactose intolerance in malnutrition has beenwell described344�4’; however, the relevance ofthis intolerance to milk feeding is controversial.

Reddy and Pershad,2 in a study evaluating amilk-based diet in refeeding programs, conclude

that this is a self-limiting problem and of littlepractical importance. An ongoing evaluation” of

a supplemental milk feeding program serving32,000 rural Haitians and an accompanying

program refeeding the severest cases of malnutri-tion (301 subjects) make the same conclusions. Afavorable outcome was reported for 93% of thesubjects in a refeeding program. Milk intolerance

could not be excluded as a possible cause offailure in only 1% of the subjects. In a studyreported by Prinsloo et al.,42 children refed on

cow’s milk did not have more diarrhea than those

fed formulas with glucose, sucrose, or D-maltose,although lactic acid excretion was high in chil-

dren fed cow’s milk.

In the study by Bowie” referred to earlier,

lactose-induced diarrhea had no effect on nitro-gen retention or fat absorption. He concludedthat, as long as milk is the most widely available

and cheapest source of good protein, it should be

used. However, he does caution that childrenwith severe diarrhea will require a lactose-free

formula for a variable period of time. Mason etal.44 reported similar tolerances.

Mitchell et al.45 reported results of blind-

controlled feeding trials evaluating prehydro-lyzed lactose milk and a reconstituted whole milk.

Thirty-five slightly undernourished Australianaboriginal infants were studied. No complicationswere seen in children fed either milk, but five of

those fed whole milk failed to gain weightcompared to only one in the hydrolyzed lactosemilk group. Children fed the hydrolyzed lactosemilk had a mean 70% larger weight gain than

those fed the whole milk. Children with diarrheaor weights less than 90% of expected weight for

age who were fed hydrolyzed lactose milk hadstatistically significant higher weight gains than

comparable groups of children fed whole milk.

The effects of previous malnutrition orgastrointestinal disease on the prevalence ofprimary lactose intolerance is difficult to evaluate

because few studies have attempted to quantitate

the severity of observed intolerance or malabsorp-tion. Paige and co-workers25 report no differences

in prevalence between previously malnourished

children and their siblings who had no history ofsignificant malnutrition, although tolerance levelsin both groups appear lower than observed inchildren in this country. Woteki et al.” found theprevalence of lactose intolerance of Mexican-Americans similar to that reported by Sowers andWinterfeldt’4 from rural Mexico. Stoopler et al.27restudied children with lactose malabsorptionseven months after an initial evaluation and found

that 21% had normal lactose tolerance curves onretesting. In Britain, no correlation was found

among continuing lactose intolerance, maximalincrease in blood glucose level after a standardlactose test dose, intestinal lactase levels, andsmall intestinal morphology on reevaluation46 of30 children 2 to 38 months old with a previous

diagnosis of presumably secondary lactose intoler-

ance.

by guest on March 18, 2021www.aappublications.org/newsDownloaded from

Page 5: The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

244 LACTOSE INTOLERANCE

Summary

Individuals using milk-based diets in refeedingprograms occasionally report initial problems

with diarrhea aggravated or precipitated bylactose. In this early phase, a hydrolyzed lactose

or lactose-free milk may be optimal. Apparently,

however, whole milk is successfully used forrefeeding, unless there is severe diarrhea. This

suggests that the milder cases seen out of the

hospital may present less significant problems.

The report by Mitchell et al.,45 however, suggeststhat the effect of lactose may be more subtle.

Although unavailable lactose may not presentmajor problems to fat and nitrogen absorption,

the decrease in metabolizable energy may be

enough to decrease the rate of weight gain,lengthen hospital stays, and therefore decrease

the effectiveness of lactose in refeeding programs,

unless compensated for in the total diet. Compar-

able studies should be repeated in hospital andsupplementary feeding programs to determinewhether or not potential effects on nutrient

bioavailability are as significant as this study

suggests.

CONGENITAL LACTOSE INTOLERANCE

The extremely low or absent activity of brush-border lactase67 in congenital lactose intolerance

can be life-threatening because of the accom-panying severe diarrhea and dehydration when

lactose is fed. The condition is rare, but it is not

unusual for secondary lactose intolerance to be

misdiagnosed during the newborn period as

congenital lactose intolerance. A definite diagno-

sis requires intestinal biospy for histology and

enzyme assay. Nonetheless, it is imperative that a

lactose-free formula be provided as soon as thediagnosis is suspected because of the seriousness

of the condition.

RECOMMENDATIONS ANDCONCLUSIONS

The Committee’s position remains unchanged.On the basis of present evidence it would beinappropriate to discourage supplemental milk

feeding programs targeted at children on the basis

of primary lactose intolerance. The Committee

continues to encourage the development of nutri-

tious and acceptable supplementary foods inareas with inefficient and uneconomical milkproduction. The use of milk should not be dis-couraged in the refeeding of malnourished chil-

dren-except if they have severe diarrhea-as long

as milk continues to provide the best and cheapest

source of high-quality protein. However, the

Committee cautions that some of these childrenwill require lactose-free diets if recovery is to be

achieved with minimal complications. It alsourges that studies such as those of Mitchell et a!.’5be continued in inpatient and outpatient facilities

for reasons outlined here; that more attention begiven to studies of environmental effects onenterocyte function, thereby increasing our

understanding of the development of low lactaselevels; and that efforts to provide effective, low-cost, supplemental foods to children be continuedas part of comprehensive health planning for

decreasing morbidity in children.

COMMITTEE ON NUTRITION

Lewis A. Barness, M.D., Chairman; Alvin M. Mauer,M.D., Vice-Chairman; Arnold S. Anderson, M.D.; Peter R.Dallman, M.D.; Gilbert B. Forbes, M.D.; Buford L. Nichols,Jr., M.D.; Claude Roy, M.D.; Nathan J. Smith, M.D.; W.Allan Walker, M.D.; Myron Winick, M.D.

REFERENCES1. PAG ad hoc working group on milk intolerance: Nt,tri-

tional implication. FAG Bull 2:7, 1972.2. Food and Nutrition Board, National Academy of

Sciences: Background Information on Lactose and

Milk Intolerance. Washington, DC, NationalResearch Council, May 1972.

3. Committee on Nutrition: Should milk drinking bychildren be discouraged? Pediatrics 53:576, 1974.

4. Jones DV, Latham MC: The implications of lactoseintolerance in children. I Trop Fediatr 20:262,1974.

5. Simoons FJ, Johnson JD, Kretchmer N: Perspective onmilk-drinking and malabsorption of lactose. Pediat-rics 59:98, 1977.

6. Asp NC, Dahlqvist A, Kuitunen P, et al: Complete

deficiency of brush-border lactase in congenital

lactose malabsorption. Lancet 2:329, 1973.

7. Freiburghaus AU, Schmitz J, Schindler M, et al: Protein

patterns of bnish border fragments in congenitallactose malabsorption and in specific hypolactasia

of the adult. �\T Engl I Med 294: 1030, 1976.8. Paige DM, Bayless TM, Mellitis ED, Davis L: Lactose

malabsorption in preschool black children. Am IClin Nutr 30:1018, 1977.

9. Garza C, Scrimshaw NS: Relationship of lactose intoler-

ance to milk intolerance in young children. Am I

Gun Nutr 29:192, 1976.

10. Paige DM, Bayless TM, Dellinger WS Jr: Relationship ofmilk consumption to blood glucose rise in lactoseintolerant individuals. Am I Clin Nutr 28:677,

1975.

11. Haverberg L, Kwon PH, Scrimshaw NS: Comparativetolerance of adolescents of differing ethnic back-grounds to lactose containing and lactose-hydro-lyzed milk: I. Initial experience with a double blind

procedure. Unpublished manuscript.12. Kwon PH, Rorick M, Scrimshaw NS: Comparative

tolerance of adolescents of differing ethnic back-grounds to lactose containing and lactose-hydro-lyzed milk: II. Experience with improved double

blind procedure. Unpublished manuscript.

by guest on March 18, 2021www.aappublications.org/newsDownloaded from

Page 6: The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

AMERICAN ACADEMY OF PEDIATRICS 245

13. Woteki CE, Weser E, Young EA: Lactose malabsorption

in Mexican-American children. Am I Clin Nutr

29:19, 1976.

14. Sowers MF, \Vinterfeldt E: Lactose intolerance amongNiexican-Americans. Ani I Clin Nutr 28:704, 1975.

15. Lisker R, Lopez-Habib C, Daltabuit M, et al: Lactose

deficiency in a rural area of Mexico. Am I Clin Nutr

27:756, 1974.16. Casky DA, Payne-Bose D, Welsh JD, et al: Effects of age

on lactose malabsorption in Oklahoma Native

Americans as determined by breath H2 analysis. Am

I Dig Dis 22:113, 1977.17. Newcomer AD, Thomas PJ, McGill DB, Hoffman AF:

Lactase deficiency: A coniinon genetic trait of the

American Indian. Gastroenterology 72:234, 1977.

18. Lebenthal E, Antonowicz I, Schwachman H: Correla-

tion of lactase activity, lactose intolerance, and milkconsumption in different age groups. Am I Clin

Nutr 28:595, 1976.19. Paige DM, Bayless TM, Ferry GD, Graham CC: Lactose

malabsorption and milk rejection in Negro children.

Iohns Hopkins Med I 129:163, 1971.20. Stephenson LS, Latham MC: Lactose intolerance and

milk consumption: The relation of tolerance to

symptoms. Ani I Clin Nutr 27:296, 1974.21. Paige DM, Bayless TM, Dellinger WS Jr: Relationship of

milk consumption to blood glucose rise in lactoseintolerant individuals. Am I Clin Nutr 28:677,

1975.22. Mitchell KJ, Bayless TM, Paige DM, et al: Intolerance of

eight ounces of milk in healthy lactose intolerate

teen-agers. Pediatrics 56:718, 1975.23. Newconier AD, McGill DB, Thomas PJ, Hoffman AF:

Tolerance to lactose among lactose deficient Amer-

ican Indians. Unpublished manuscript.24. Bayless TM, Rothfeld B, Massa C, et al: Lactose and

milk intolerance: Clinical implications. N Engl IMed 292:1156, 1975.

25. Paige DM, Leonardo E, Nakashima J, et al: Response oflactose intolerant children to different lactose

levels. Am I Clin Nutr 25:467, 1972.

26. Reddy V, Pershad J: Lactase deficiency in Indians. Am I

Clin Nutr 25:114, 1972.27. Stoopler M, Frayer W, Alderman MH: Prevalence and

persistence of lactose malabsorption among youngJamaican children. Am I Clin Nutr 27:728, 1974.

28. Jones DV, Latham MC, Kosikowski FV, Woodward C:Symptom response to lactose-reduced milk inlactose-intolerant adults. Am I Clin Nutr 29:633,1976.

29. Paige DM, Bayless TM, Huang 55, Wexler R: Lactosehydrolyzed milk. Am I Clin Nutr 28:818, 1975.

30. Marston R, Friend B: Nutritional Reeiew, National Food

Situation, publication NFS-158. Economic Re-

search Service, US Dept of Agriculture, Nov 1976,

p 25.

31. Galloway DH, Chenoweth WL: Utilization of nutrients

in milk and wheat-based diets by men with

adequate and reduced abilities to absorb lactose: I.Energy and nitrogen. Am I Clin Nutr 26:939,1973.

32. Leichter J, Tolensky AF: Effect of dietary lactose on theabsorption of protein, fat, and calcium in the

postweaning rat. Am I Clin Nutr 28:238, 1975.33. Bowie MD: Effect of lactose-induced diarrhoea on

absorption of nitrogen and fat. Arch Dis Child

60:363, 1975.

34. Bowie MD, Barbezat GO, Hansen JDL: Carbohydrate

absorption in malnourished children. Ani I Clin

Nutr 20:89, 1967.

35. Kabayashi A, Kawai 5, Ohbe Y, Nagashima Y: Effects ofdietary lactose and a lactase preparation on theintestinal absorption of calcium and magnesium innormal infants. Am I Clin Nutr 28:681, 1975.

36. Cook CC, Al-Torki MT: High intestinal lactase concen-

trations in adult Arabs in Saudi Arabia. Br Med I3:135, 1975.

37. Cook CC, Kajubi 5K: Tribal incidence of lactase defi-

ciency in Uganda. Lancet 1:725, 1966.38. Kretchmer N, Ransome-Ksiti 0, Hurwitz R, et al:

Intestinal absorption of lactose in Nigerian ethnic

groups. Lancet 2:392, 1971.39. Kretchmer N: Lactose and lactase. Sci Am 227:71, Oct

1972.40. Keusch C, Troncale FJ, Thavaramara B, et al: Lactase

deficiency in Thailand: Effect of prolonged lactose

feeding. Am I Clin Nutr 22:638, 1969.

41. Bowie MD, Brinkman GL, Hansen JDL: Acquired

disaccharide intolerance in malnutrition. I Pediatr66:1083, 1965.

42. Prinsloo JC, \Vittrnann W, Pretorius PJ, et al: Effect of

different sugars on diarrhea of acute kwashiorkor.

Arch Dis Child 44:593, 1969.43. Marshall FN, Hilaire JA, Gamier MJ: Personal coinmu-

nications.

44. Mason JB, Hay RW, Leresche J, et al: Treatment of

severe malnutrition in relief. Lancet 1:332, 1974.45. Mitchell JD, Brand J, Halbisch J: Weight-gain inhibition

by lactose in Australian Aboriginal children: A

cotrolled trial of normal and lactose hydrolysedmilk. Lancet 1:500, 1977.

46. Harrison M, Walker-Smith JA: Reinvestigation oflactose intolerant children: Lack of correlationbetween continuing lactose intolerance and smallintestinal morphology, disaccharidase activity and

lactose tolerance tests. Gut 18:48, 1977.

by guest on March 18, 2021www.aappublications.org/newsDownloaded from

Page 7: The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

1978;62;240Pediatrics The Practical Significance of Lactose Intolerance in Children

ServicesUpdated Information &

http://pediatrics.aappublications.org/content/62/2/240including high resolution figures, can be found at:

Permissions & Licensing

http://www.aappublications.org/site/misc/Permissions.xhtmlentirety can be found online at: Information about reproducing this article in parts (figures, tables) or in its

Reprintshttp://www.aappublications.org/site/misc/reprints.xhtmlInformation about ordering reprints can be found online:

by guest on March 18, 2021www.aappublications.org/newsDownloaded from

Page 8: The Practical Significance of Lactose Intolerance in Children · Nevertheless, controversy over the practical significance of the widespread preva-lence4’5 of lactose intolerance

1978;62;240Pediatrics The Practical Significance of Lactose Intolerance in Children

http://pediatrics.aappublications.org/content/62/2/240the World Wide Web at:

The online version of this article, along with updated information and services, is located on

American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397. American Academy of Pediatrics, 345 Park Avenue, Itasca, Illinois, 60143. Copyright © 1978 by thebeen published continuously since 1948. Pediatrics is owned, published, and trademarked by the Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it has

by guest on March 18, 2021www.aappublications.org/newsDownloaded from