Stephen Robyn

JD O’Keeft, Elizabeth Lavender, and Trevor

(24

A O’Keefe, Kemp

Fifty malnourished

ABSTRACT randomly

assigned

to whole

g lactose/L),

constant ofintolerance

lactose-free

infusion

to 3 L/d

for

iftolerated.

in 63%

ofpatients

whole

and

milk

cretion

on day

fed patients in all three

receiving

and

high

products

excretion

tive.

AmfClinNutr

KEY

such

rates

milk,

weights

in the

were

and

in-

symptoms 37%

and

associated

milk

may

prove

Milk,

malabsorption,

malnutrition, breath

Africans,

hydrogen,

effec-

studies

throughout

cans, especially those of the polactasia, ie, after weaning, intestine

diminishes

in rural

change

Bantu the

that

depletions

are

of hospitalized

significant

patients

from

between strong

proportions situation

in most impoverished recently being exacerbated

ciency syndrome American and supplements hand, milk whole food nearly

(AIDS). European

rural

form store

fore, should we avoid nourished Africans? 130

Studies to show

ingestion

stores

of of 50

African

populain

patients

300 g/d, However,

given containing despite

the

and

as-

African communities (9), the by acquired immune deficontrast to the situation lactose-free nutrient-dense

consequently

in South giving

Africa. milk

or

can

be obtained

The

question

milk

products

in

from is, thereto

Am J C/in Nutr

the

in the form

as part

before cause

provision ofdrinks

taken

of a mixed

taste

every

enjoyed

diet.

Fresh

4 h, induced

had

by both milk

a stool

weight

to completely it was

noted

rural

and

urban

popular

than

is less

that

practice is either to purchase com(maas) or allow milk to sour naturally

This of sour

who

because

and

milk

and nitrogen (10). Fecal 24 g fat, in comparison

diet

of milk

and

of energy-dense

6.8 g fat. it was difficult

value

African milk

on average these results

consumption. the

giving

a lactose-free

potential

was commonly

practice

milk

given

as a simple

could

was

have

preferable

arisen

either

or because

drink

to samples

beit was

as an appropriate Africans if the rate constant

enteric

Subjects

and

the present low-lactose

liquid-formula of intake was

to 17

of malnourished

different rural districts of South Africa ofsymptoms to be only 10%. Encouraged

results we then undertook that milk, or a modified

Patient

and pulmonary tuberculosis was tuberculosis has reached epidemic

In sharp hospitals,

that

sour milk and the general mercial sour-milk products

70%

(6, 7). The

given

avoid

and

found by these

study to test the hypothesis milk product, could be used

diet for malnourished reduced to the form

rural of a slow,

infusion.

any

are unavailable because of expense. On the other forms a versatile supplement and is the cheapest available. It lends itself well to transportation and

in dried every

malnutrition (6-8) and

the

Afri-

primary hyin the small

(1-4).

in body populations

that

failed

in rural

these

sociation particularly

90% after

common

there

>

concentrations

tions

and

shown

amounts

demonstrated glucose

have

we found

diets,

lactose-intolerant

we should

diarrhea and malabsorption offat was 1 kg/d, containing on average

g lactose)

methane

subgroup, have lactase activity

to insignificant

Zulus

in blood

Africa

g lactose in solution (5). Malnutrition is extremely

storage

severe weight

that

better tolerated in the same way that yogurt has been shown be better tolerated by lactose-intolerant Americans (1 1). We (12) tested the tolerance to 350 mL milk (containing

Introduction

ours

milk-based

patients from the incidence

Numerous

in 40 malnourished

because

blacks

better

hypolactasia,

breath

products,

milk

positive methane

cost

studies suggested

disregard

suggest that although undiluted cow tube feed for malnourished African

as acidified

Initial




1 L stool

could

of steatorrhea

..

during

easily

the

be identified

-

24-h

weight,

period.

group outputs diet, milk, The

by eye (Fig 4).

excreting

patients whole given

>

Measurement absorption was 2 g N. Thus,

with

milk,

excretion

(16.6

modest

calculated

milk,

pa-

excreting

a net fat content with only

nitrogen

electrolytes

balance,

demonstrated

the lactose-free increases

± 14 and

consuming

three

indicating

of the nitrogen less impaired,

consuming

only

in two

on the acidifiedmilk. The degree

positive in all three groups, the presence of severe diar-

of stool

for those

in those

steatorrhea

in five receiving in those

measurement

diets,

secretory

1 7.6

± 7.8

indicating

and

in sodium mmol/d,

osmotic

acid-

and

po-

respecrather

than

diarrhea.

hydrogen

Although breath

70%.

only

excretions

tassium

Breath

demonstrated

limits

25 g) in the 24-h-period,

>

protein

Finally,

tively)

the upper

in Table 4, was markedly those given milk, despite

ified-milk

details

(ie, of

in one patient

fat content

was far greater

70 mmol

absorption

groups.

line demonstrates

tients milk

similar

Twenty-four-hour

dotted

MILK

Analysis

>

of2.8 L diet (Table lactose-free group

from

the

only This

one on day 3) and

On the third

group,

seen

formulas.

results

1’-

;-

and methane

there

hydrogen

day

ofinfusion,

those

given

were and the

milk

.

no significant methane

differences

concentrations

concentrations

(44.8

..

concentrations

± 20 ppm)

in group during

ofhydrogen but

were

were very

.

FIG 4. Stool samples obtained from the three groups of patients. From left to right, the first four samples were obtained from patients given the acidified-milk formula, the middle six were derived from those receiving whole milk, and the four on the right were obtained from those receiving the lactose-free diet. The presence of steatorrhea in those given the milk diet is obvious.

mean

the second highest

similar

in

in the

Downloaded from https://academic.oup.com/ajcn/article-abstract/54/1/130/4690953 by McMaster University user on 11 February 2019

3

134

O’KEEFE

TABLE 4 Estimated nitrogen

ET

AL

TABLE 5 Breath hydrogen

balance Milk

Acidified

milk

Lactose-free

results

during

50-g lactose-tolerance

Milk

diet

Acidified

milk

14.5

±

2.5

1.4± 1.3 +7.4 ± 3.4

diet

± 0.5

15.0 ± 2.0

Oh

35±25

23±14

16±10

4.6 ± l.3 0.8±0.5 +3.1 ± l.3t

7.0 ± 3.2 0.7 ±0.4 +7.2 ± 3.9

lh

62±40

61±52

30±24

2h

76±67

62±65

57±46

8.5

± 1.9

5.7

Lactose-free

ppm

g/d Diet Urine Feces Balance

tests

tt Significantly

different

from

lactose-free

diet: tP

0.005,




of patients

that

excretion

in breath

cretors

per-

of symptoms

increased

all but two ofthese individuals tolerated as well as 50 g oral lactose at the end elevations

patients distension

6). It was

and of

hydrogen

were in 87%

ingestion

concentrations

breath

the

of the

these

that

of its lactose

are reproduced solution.

free diets

concentrations

varied

in all

75% but

complained

of abdominal

concentrations

by lactose

and

symptoms sociated

of the

assumed

is a consequence

in simple

stool.

methane

among

because

those

similar

20 ppm,

>

values increase

percent

group,

an increase

primarily

very

Ninety

acidified-milk

showed

of a loose

rates

It is generally

test at the end the baseline milk, the

2 h was

41 ppm.

the test 38% ofpatients

of intolerance, Breath

next

be underestimates

During

passage

the

39 and

7 1% of the group

centages fasting.

over

between

lactose-free

fected

lactose-

feeding

of day 3 are shown in Table 5. Although were again highest in those who had received

milk

and

35 ± 12 ppm).

13 7

16 10

1 4

1 47

3

2

1

6

7

7

5 36

5 42

5

7

21

#{149}5

5

6

l5

36

10

22

*6

6

6

*35

37

45

49

52

*7

*3

6 4 11

32

5 10

6

4

#{149}7

8

11

13 2 9

15 2 3

2 13 16

4 7 18

11 16

5

7

5

24

5

5

16

31

40

30 17

39

61

42

44

0

5

5

10

3

4

6

7

5

*3

7

7

7

11

7

25

19

19

C

6 7

Patients

with more

*7

than

three

loose stools

per day on day 3.

Downloaded from https://academic.oup.com/ajcn/article-abstract/54/1/130/4690953 by McMaster University user on 11 February 2019

SD.

I

SD.

C

MILK-INDUCED of6O% in normal volunteers given conventional mula diets, the diarrhea being reversed by pectin

MALABSORPTION

lactose-free administration.

for-

However, in contrast to the situation for the patients given the diarrhea in the lactose-free group gradually improved the

3 d and

was

not

generally

associated

with

milk, over

nutrient

malab-

sorption.

1. Cook GC, Kajubi SK. Tribal incidence of lactase deficiency in Uganda. Lancet 1966;l:725-9. 2. Kretchmer N, Ransome-Kuti 0, Hurwitz R, Dungy C, Alakija W. Intestinal absorption of lactose in Nigerian ethnic groups. Lancet

that

quantity

“in

oflow

However,

symptomatic

lactose

could

have

by acidification,

that

infants.

in decreased

acid

helps

tors might

involve

taminant

shown

growth

after

to suppress

Less

with

study

who

either

that

in the

Acidification

subsequent

colonic

has been

tolerated

is low

also

acidified

results

milk

feed

sim-

Further

fac-

on con-

before

infusion

or

oflactose

drinks

was

production

of hydrogen

(19).

paid

hypolactasia

secretion

effect ofacidification

individuals

attention

viduals

the

are increased

malnutrition

infusion.

in lactose-intolerant

Furthermore

circumstances.

the suppressive

bacterial

in the intestine

these

for in-

and reduced

gastric-acid

it is possible

in

tolerance.

digestibility

severe

under

reduction

designed

milk.

and

because

secretion,

the

improved

originally

to human

Because

digestibility

than

carbohydrate,

tolerance

presumably

in premature

was

greater

can be consumed.”

for the

increased

similar

claim

milk

other

used

protein,

is more

manufacturers

ilarly

factors

diet could have et al (18), who

a significantly

regular

responsible

product

The reduced content

than

that

been

acidified-milk

fants.

subjects,

milk

it is possible

lactose The

tolerance to the acidified-milk from the study of Veale Jones

to the reasons

(eg,

the

3 L milk)

four

can

why

patients

tolerate

some

in the

large

mdi-

present

quantities

of

milk. An attractive explanation would involve the increased vage capacity by colonic bacteria. The association we found tween

good

indicate

milk

a role

tively,

tolerance for

methane

tients

with

ation

between

diarrheal

production

producers

remained

previously

drew

attention

common ation

by Segal fact

by cow

viduals

product

bedside

methane

with

was equal

measures

for

and

to improve

milk

and

We

thank

Nick South

Partington, Africa,

for

colon

tolerance

feeding

malnour-

some

of the to assess

tolerance

[eg, lactis

mdi-

low-lactose

expensive

needed

with

cancer.

malabsorption

However,

Nutritional his support

associ-

use as an alternative tube

galactosidase enzyme from Kluyveromyces reduce reliance on commercial manufacturing

hannesburg,

rates un-

proposed

and

of the more are

high

in addition,

is relatively

the

tuberculosis.

trials

of methane

Similar

cancer

and

on breath

incidence

at 87%.

its general

to that

clinical

production

et at (2 1), who,

diets

in paan associ-

purgation

production

3 L milk/d

Further

noted

of symptoms

precludes

patients

suppressed

disputing

severity

milk

been

colonic

liquid-formula

tolerated diet.

that

Alterna-

studies

the high

therefore

the

African

milk

However,

increased

to commercial ished

(20).

exceptionally

might

regard.

low methane

of mechanical

to the

between

have

and

production

in this

previous

states

reported

In conclusion,

methane

effect

in Africans,

induced

might

because

also the suppressive methane

high bacteria

production

diarrhea,

were

and

methogenic

salbe-

lactosethe

the

use

use

(22)] and processes.

Advisor, Nestl#{233} Ltd, the study.

of

of /3thus

B Jo-

3. Jenkins T, Lehmann H, Nurse GT. Public health and genetic constitution of the San (“Bushmen”): carbohydrate metabolism and acetylator status of the Kung of Tsumkwe in the North-western Kalahari. Br Med J l974;2:23-6. 4. Jersky J, Kinsley RH. Lactose deficiency in the South African Bantu. S Afr Med J 1967;4l:l 194-6. 5. O’Keefe SJD, Adam JK. Primary lactose intolerance in Zulu adults. S Afr Med J l983;63:778-80. 6. O’Keefe SJD. Malnutrition among adult hospitalized patients in Zululand during the drought of 1983. S Afr Med J l983;64:628-9. 7. O’Keefe SJD, Rund JE, Marot NR, Symmonds KL, Berger GMB. Nutritional status, dietary intake and disease patterns in rural Hereros, Kavangos and Bushmen in South West Africa/Namibia. S Afr Med J 1988;73:643-8. 8. O’Keefe SJD, Thusi D, Epstein S. The fat and the thin-a survey of nutritional status and disease patterns among urbanized Black South Africans. S Afr Med J 1983;63:679-83. 9. O’Keefe SJD, Lavender R. The plight of the modern Bushmen. Lancet l989;2:255-8. 10. O’Keefe SJD, Adam JK, Cakata E, Epstein S. Nutritional support of malnourished lactose intolerant African patients. Gut l984;25: 942-7.

1 1. Kolars JC, Levitt MD, Aouji M, Savaiano DA. Yogurt-an autodigesting source oflactose. N Engi J Med l984;3lO: 1-3. 12. O’Keefe SJD, Young GO, Rund J. Milk tolerance and the malnourished African. Eur J Clin Nutr 199O;44:499-5O4. 13. Newcomer AD, McGill DB. Clinical importance oflactose deficiency. N EngI J Med 1984;3l0:42-3. 14. Scrimshaw NS, Murray EB. Lactose deficiency and the absorption ofnutrients. Am J Clin Nutr 1988;48:ll26-8. 15. Keohane PP. Attrill H, Love AR, et al. Relations between osmolarity of diet and gastrointestinal side effects in enteral nutrition. Br Med J 1984;288:678-8O. 16. Kelly TWJ, Patrick MR. Hillman KM. Study ofdiarrhea in criticallyill patients. Crit Care Med 1983;l 1:7-9. 17. Zimmaro DM, Rolandelli RH, Koruda MJ, Settle RG, Stein TP, Rombeau JL. Isotonic tube feeding formula induces liquid stool in normal subjects: reversal by pectin. JPEN 1989;l3: 1 17-23. 18. Veale Jones D, Latham MC, Kosikowski P1, Woodward G. Symptom response to lactose-reduced milk in lactose-intolerant adults. Am J Clin Nutr 1976;29:633-8. 19. Perman JA, Modler S, Olson AC. Role of pH in production of hydrogen from carbohydrates by colonic bacterial flora. Studies in vivo and in vitro. J Clin Invest 198 1;67:643-50. 20. Peled Y, Weinberg D, Hallak A, Gilat T. Factors affecting methane production in humans. Gastrointestinal diseases and alterations of colonic flora. Dig Dis Sci 1987;32:267-7l. 21. Segal I, Walker ARP, Lord S. Cummings JH. Breath methane and large bowel cancer risk in contrasting African populations. Gut 1988;29:608-l 3. 22. Rosado JL, Morales M, Pasquetti A. Lactose digestion and clinical tolerance to milk, lactose-prehydrolysed milk and enzyme added milk: a study in undernourished continuously enteral-fed patients. JPEN l989;l3:157-61.

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concluded

free

References

197 1;2:392-5.

The improved been predicted

fat

135