Dietary approaches to alleviation of lactose maldigestion Efectos de

Transcripción

71
Dietary approaches to
alleviation of lactose
Efectos de la dieta sobre la
maldigestion
digestión de la lactosa
E. Renner
Dairy
Science Section,
Justus Liebig University, Bismarckstr. 16, 35390 Giessen, Germany
Because dairy products are a significant source of essential nutrients, elimination of all dairy foods
in the diet would be nutritionally unwise and is usually not necessary in the case of lactose
maldigestion. About 250 ml milk/d can generally be taken without adverse effects. If milk is taken
in combination with solid foods, lactose malabsorption may be reduced by about 50%, probably
due to a slower rate of colonic fermentation which may lower gastrointestinal symptoms in lactose
malabsorbers. It is well established that, in lactase-deficient subjects, yoghurt is better tolerated
than milk. This is only to some extent related to the fact that the lactose content of the products
is reduced during fermentation, but is mainly attributed to the fact that the culture organisms by virtue of being rich in lactase - are able to participate in the hydrolysis of ingested lactose.
Up to 20 g of lactose in yoghurt is tolerated well by lactase-deficient persons. The enhanced absorption of lactose in yoghurt is explained as a result of the intestinal release of lactase from the
yoghurt organisms. Ripened cheese is also tolerated very well by lactose-intolerant persons since
virtually all of the lactose present is decomposed to lactic acid and other metabolites.
Keywords: diet, lactose, maldigestion, dairy products
Los productos tacteos son uno fuente signific<:ltiB’a de nutrientes esenciales por ellu, la eliniinicic)ii
de los productos licteos de la dieta no es aconsejabte y tampoco necesario en el caso de la mala
digestion de la lactosa. Diariamente pueden ingerirse, aproximadamente 250 ml de leche sin efectos
adversos. Si la leche se ingiere con alimentos s6lidos, la mala absorci6n de la lactosa puede
reducirse hasta un 50%, debido probabiemente a la lenta velocidad de la fermentacion en el colon,
]0 cual hace clue los sintomas u’wlStr-lllrlte5tltldlCS disntinuyan en las personas con una mala absorcidn de la lactosa. Es de sobra sabido, que las personas que absorben mal la lactosa, toleran mejor
Cl yogur. Esto no es s6to porque el producto en si contenga la lactosa parcialmente hidrolizada,
sino porque los microorganismos presentes en el yogur - por estar enriquecidos con lactasa- son
capaces die participar en la hidr6)isis de li lactosa ingerida. Las personas que absorben mal la
lactosa pueden toterar bien hasta 20 g de lactosa en el yogur. El incremento de la absorcion de la
lactosa del yogur se explicar por el aportc de lactasa en el intestino proveniente de los microorganismos presentes en el yogur. El queso curado se tolera muy bien debido a que practicaniente
toda la lactOSc’1 se ha transformado en 6cido lictico y otros metabolitos.
Palal¡/&dquo;tIs clrrm·: dieta, lactosa,
indigestion, productos
licteos
water to enter the lumen of the intestine. The
I NTRODUCTIO N
causes
Lactose maldigestion is caused by a considerably
reduced lactase activity in the mucosa of the small
intestine. As a result, lactose is not split, and the
increase in the lactose concentration inside the intestine produces an increased osmotic pressure which
lence, colic, and diarrhoea. In young mammals, the
resulting symptoms
are
abdominal pressure, flatu-
activity falls after VB/eaning, which suggests
adaption to the absence of lactose. About 90% of
human adults in the world show some degree
lactase deficiency.
lactase
Downloaded from fst.sagepub.com at SAGE Publications on December 6, 2012
an
all
of
72
It is necessary to differentiate between lactose
malabsorption and lactose intolerance, which were
defined as follows by Solomons (1986): (i) Lactose
malabsorption is the incapacity to quantitatively digest an oral dose of lactose into its constituent simple
sugars (glucose and galactose) during its passage
through the small intestine. The diagnosis is made by
objective measures of the failure to take up the carbohydrate from the gut; (ii) Lactose intolerance is the
experience of symptoms of gastrointestinal discomfort which have already been mentioned.
Frequency
of lactose
maldigestion
Lactose malabsorption usually can be found in adults
at the end of the growth period. There are considerable differences between various ethnic groups. The
ability to retain a high lactase ability during the whole
of one’s life seems to be the result of a mutation which
occurred several thousand years ago. The reason for
the lactose tolerance is thought to be selection pressure for ecological reasons; for instance, lactose would
increase calcium absorption in an environment with
low UV radiation and a low vitamin D supply in
the diet (Simoons, 1978). Lactase deficiency is genetically determined. Man differs from other mammals
in that some subjects continue producing lactase after
infancy and throughout adult life (Cavalli-Sforza
et al. 1987).
Less than 10% of the adult population in Central
and North Europe, North America and Australia and
20-40% of people in the Mediterranian countries are
affected by lactose malabsorption, while in Africa,
Asia and South America and in some other ethnic
groups, the majority of the adult population suffers
from lactase deficiency.
Lactose tolerance test
the breath hydrogen test is used to assess
digestion. This test is based on the fact that
lactose, which is not absorbed in the small intestine
(because of a lactase deficiency), reaches the colon,
where bacterial fermentation produces hydrogen gas
as one of the resulting products; the hydrogen is
partly absorbed by diffusion into the blood stream
and expired in the breath (Berg et al., 1985). In the
breath hydrogen test, the concentration of hydrogen in expired air is determined at fixed intervals.
Figure 1 shows the changes in breath hydrogen
concentration after ingestion of 360 ml of milk (18 g
of lactose) by lactose absorbers and lactose malabsorbers. An increase in hydrogen concentration of >
20 ~.1/L above basal values during the 5 h interval
Usually
lactose
post-ingestion changes in breath hydroconcentration after ingestion of 360 ml of milk
(18 g of lactose) by lactose-absorbers (LA) and lactosemalabsorbers (LM) (from Rosado and Solomons, 1983).
Figure
gen
1. Mean
(H2)
Figura 1. Cambios en la concentraci6n del hidr6geno
eliminado en la respiraci6n despu6s de la ingestion de
360 ml de leche (18 g de lactosa) por personas que
absorben la lactosa (LA) y las que no (LM) (datos segun
Rosado y Solomons, 1993).
after
ingestion indicates the occurrence of lactose
malabsorption (Rosado and Solomons, 1983).
For the lactose tolerance test, originally a standard
dose of 50 g lactose in an aqueous solution was used.
This dose was too high, and a test using such a dose
is therefore of no particular value in the detection of
lactose intolerance. Furthermore, the lactose should
not be administered in an aqueous solution but in its
natural food form (milk); lactose in water produces
more severe symptoms than lactose in milk. In a study
conducted by Sategna-Guidetti et al. (1989) it was
observed that, when 25 g of lactose were applied in
500 ml of whole milk, only 8% of the population
developed symptoms of lactose malabsorption as
indicated by a breath hydrogen rise of more than
20 ppm, whilst 33% showed signs of lactose malabsorption when the same amount of lactose was
administered in aqueous solution. It has therefore
been proposed that the lactose tolerance test should
be carried out with a physiological dose of lactose
of 12 g which is the amount contained in a glass of
milk, and that milk should be used as the natural
source of lactose (Renner, 1983).
Dietary
measures
dietary approaches to alleviation of lactose
maldigestion are discussed it has to be emphasized
When the
73
could
nutritional status (Saavedra and
day can generbe
taken
If
vvithout
adverse
effects.
ally
necessary, the
milk can be consumed in several small portions
spread throughout the day.
Several other dietary approaches, such as lowlactose or lactose-free dairy products (ripened cheese),
low-lactose milk obtained by ultrafiltration or lactose
hydrolysis, cultured dairy products, and the effect
of adding solid foods to a meal with milk, will be
discussed in more detail.
compromise
Perman, -1989). About 250 ml milk per
z
DIETARY APPROACHES
Figure 2. Change in breath hydrogen over 4
consumption of milks with reduced amounts of
h after
lactose
(from Brand and Holt, 1991).
2. Cambios en la concentraci6n del hidr6geno
eliminado en la respiraci6n despu6s de 4 horas de haber
ingerido leche con cantidades reducidas de lactosa
(datos segun Brand y Holt, 1991).
Figura
Cheese
as a
lactose-free
dairy product
On average, milk contains 4.8% lactose. The lactose
content of yoghurt (4.0%) and other cultured dairy
products is reduced by about 20% due to lactic acid
fermentation, if the milk is not pre-concentrated.
Ripened cheeses, hard cheese as well as semi-hard
and soft cheese, have only traces of lactose as most
of the lactose in milk is transferred into the whey and
the residual lactose is fermented. Therefore, ripened
cheese represents an ideal food product in the diet of
the lactose malabsorber. On the other hand, fresh
cheese contains about 3.7% lactose, and also processed
cheese is not lactose-free (4% lactose) because milk
powder or whey powder are usually added during
the manufacturing process (Renner and Renz-
Schauen, 1992).
Low-lactose milk
Low-lactose milk can be obtained by lactose hydrolultrafiltration. It is not necessary to remove
the lactose completely. Brand and Holt (1991)
observed that the mean maximum breath hydrogen
rise after the consumption of 300 ml of normal milk
was 31 ppm, but only 5-8 ppm when the same
amount of milk was consumed where the lactose
content was reduced by 50, 80 or 95% (Figure 2). The
results suggested that a 50% level of lactose reduction in milk may be adequate to relieve the signs and
symptoms of milk intolerance in the majority of
healthy adults with lactose malabsorption. This was
confirmed in experiments conducted by Brand Miller
and Munro (1992) who fotmd that 200 ml of normal
milk could be consumed before breath hydrogen
rose more than 20 ppm, but 500 ml of 50% lactosereduced milk could be consumed with the same effect
(Figure 3). Normal milk produced significantly more
symptoms at all levels than the 50% reduced milk.
ysis or by
Figure 3. Peak rise in breath hydrogen recorded within
3 h of consumption of graded levels of 50% lactosereduced milk and normal milk (from Brand Miller &
Munro, 1992).
Figura 3. Variaci6n del hidr6geno eliminado en la
respiraci6n registrado durante las 3 primera horas
despu6s de la ingestion de diferentes cantidades de
leche normal y leche
con
un
50%
menos
de lactosa
(datos segun Brand Miller y Munro, 1992).
that it is absolutely not necessary to exclude lactose
from the diet, as substantial numbers of individuals
with primary lactose malabsorption can consume
nutritionally significant amounts of milk without
developing intolerance. Totally eliminating milk or
dairy products from the diet of these individuals
74
lysing milk by incubation for a period of 12-24 h prior
to consumption; other enzyme preparations can be
added just before ingestion of milk. In another procedure, lactase is aseptically added after the UHT
process; in this case, milk lactose is hydrolysed to
Figure
4. Effect of
breath
a
~3-galactosidase preparation on
challenge
hydrogen excretion after a 50 g lactose
(from DiPalma and Collins, 1989).
4. Efecto de un preparado de (3-ga!actos)dasa
sobre la eliminaci6n de hidr6geno en la respirac16n
despu6s de la ingestion de 50 g de lactosa (datos segun
DiPalma and Collins, 1989).
Figura
.
Figure 5. Effect of a commercial prepration of [3galactosidase on breath hydrogen concentration compared with the ingestion of lactose-prehydrolysed milk
(from Solomons
et
al., 1985).
Figura 5. Efecto de un preparado comercial de l3-galactoxidasa sobre la concentraci6n de hidr6geno en
comparaci6n con la ingestion de leche con lactosa
prehidrolizada (datos segun Solomons et al., 1985).
These results suggest that milk with as little as 50%
lactose reduction can play a major role in the diet of
individuals with lactase deficiency.
Lactose in milk can be hydrolysed by adding the
enzyme lactase (¡3-galactosidase) which can be obtained from microorganisms. Lactase preparations
are commercially available that are effective in hydro-
about 90% after 10 d storage at room temperature.
Under very cool conditions, such as 0 °C, hydrolysis
will not go beyond 75% and takes longer to do so.
Payne et al. (1981) conducted a study where milk
to which the lactase preparation had been added
was refrigerated for 20-24 h at 4 °C so that the lactose
was at least 90% hydrolysed. While the breath
hydrogen concentration rose by about 60 ppm after
the administration of 480 ml of low-fat milk to lactose malabsorbers, no change in the breath hydrogen concentration occurred when 480 ml of low-fat
lactose-hydrolysed milk was supplied.
In experiments performed by DiPalma and Collins
(1989) p-galactosidase capsules
were
given orally
as
250 mg or 500 mg dose just before ingestion of 50 g
lactose dissolved in water. The enzyme can produce
a significant reduction in breath hydrogen excretion
when given as a 500 mg dose just before ingestion of
lactose by lactose malabsorbers (Figure 4).
Solomons et rrl. (1985) observed that adding 2 g
of a commercial preparation of f3-galactosidase from
Kluyvcl&dquo;Ol1lYces lactis at mealtime to 360 ml milk taken
with a solid food meal (breakfast cereals) reduced the
production of excess breath hydrogen attributable to
lactose maldigestion to a level not significantly different from that achieved with lactose-prehydrolysed
milk (Figure 5). Thus, exogenous [3-galactosidase can
eliminate lactose malabsorption in lactase deficient
individuals even in the presence of solid foods, allowing lactose intolerant persons to consume milk and
dairy products without gastrointestinal discomfort.
In experiments conducted by Lybeck Sbrensen
et rrl. (1983), the lactose content of skim milk was
reduced by 86% by ultrafiltration. The tolerance of
this low-lactose milk was compared with regular
skim milk in adult Latin Americans with lactose
malabsorption. The ingestion of 500 ml of the lowlactose milk gave rise to significantly fewer symptoms
(such as bloating and abdominal cramps) than regular
skim milk. It is suggested that such a low-lactose milk
might be useful in the treatment of protein-calorie
malnutrition in developing countries where lactose
malabsorption is prevalent.
a
Combining milk with
a
meal
Martini and Savaiano (1988) examined whether the
combination of milk with a meal has a favourable
effect on lactose digestion. They found that peak
75
Figure 6. Change in concentration of breath hydrogen
after ingestion of an aqueous lactose solution, a milk
based food supplement and a meal plus the supplement
Figure
7.
Change
of lactose, milk,
et
in breath
yoghurt
or
hydrogen after ingestion
lactulose (from
Kolars
al., 1984).
(from Martini and Savaiano, 1988).
Figura 6. Cambios
respiraci6n despu6s
el hidr6geno eliminado en la
de la ingestion de una disoluci6n
acuosa de lactosa, de un preparado 16cteo y de un
alimento m6s el preparado (datos segun Martini y
en
eliminado en la respiraci6n despu6s de la ingestion
de lactosa, yogur o lactulosa (datos segun Kolars
et
al., 1984).
Savaiano, 1988).
hydrogen production after a milk based food supplement was delayed 2 h as compared with a lactose
solution. Addition of a breakfast meal further delayed
peak hydrogen production by 1 h; hydrogen production was significantly lower for the first 4 h after
ingestion of the supplement plus meal compared with
the supplement alone (Figure 6). Number and severity
of symptoms was significantly reduced with the
ingestion of the supplement compared with an equal
lactose load and was further reduced with the
consumption of food, presumably due to delayed
gastric emptying. Thus, lactose malabsorbers should
consume food simultaneously with lactose-containing
beverages to reduce intolerance symptoms.
Cultured
ingested
dairy products
As to the effect of cultured
dairy products
on
lactose
et al. conducted
early
digestion,
breath hydrogen measurements in order to determine
whether lactase-deficient subjects absorbed lactose in
as
as
1984, Kolars
better than lactose in milk. Ingestion of 18 g
of lactose in yoghurt resulted in only about one third
as much hydrogen excretion as a similar amount
of lactose in milk or water (Figure 7), indicating
a much better absorption of lactose in yoghurt.
Ingestion of yoghurt also resulted in fewer reports of
diarrhoea or flatulence than did a similar quantity
of lactose ingested in milk or a water solution. Therefore, yoghurt was called an ’autodigesting’ source of
yoghurt
lactose by these authors, which makes it a well-tolerated milk product for lactase-deficient persons and
may explain the widespread consumption of yoghurt
by lactase-deficient population groups.
The enhanced absorption of lactose in yoghurt
is explained as a result of the intraintestinal digestion
of lactose by lactase released from the yoghurt organisms. As demonstrated by the analysis of duodenal samples obtained after yoghurt ingestion, the
bacterial lactase in yoghurt survives the passage
through the stomach in lactase-deficient persons. The
lactase activity would have been sufficient to digest
50-100 % of the lactose content of the samples.
Therefore it is concluded that presumably this lactase
activity substitutes for the lack of endogenous lactase
and accounts for the improved absorption of lactose
in
yoghurt (Kolars et al., 1984).
Strain differences
It has to be acknowledged that there are differences
between species and strains of lactic acid bacteria
which are used for the manufacture of cultured dairy
products. For example, the effect of various strains
and species of lactic acid bacteria was investigated
by Martini et n.I. (1991b). They included in their
study yoghurts containing mixtures of strains of
the common yoghurt culture as well as fermented
milks containing individual species of Streptococcus
tlzermoplzilus, Lactobacillus bulgaricus, L. acidophilics or
Bifidobacteriu11l bifidum that varied in microbial
76
lactose digestion must be addressed. To answer
this question, Lin eat al. (1991) administered yoghurt
and sleet acidophilus milk containing 1 x 107 or
1 x 10H cfu/ml of S. tltorttuyhiltts and L. bulgaricus,
or L. ncidophiltts, respectively, to maldigesting humans. The yoghurt milk containing 1 x 108 cfu/ml
contained significant concentrations of [3-galactosidase ; breath hydrogen peaks were significantly lower
than control values (20 vs 70 ppm at 4 h) and intolerance symptoms were eliminated in all subjects.
Yoghurt milk containing 1 x 107 cfu/ml was only
marginally different in its breath hydrogen values
from control values. As for acidophilus milk, only one
strain of L. acidophiliis was capable of significantly
decreasing breath H2 values when 1 x 108 cfu/ml of
milk was consumed. These results lead to the conclusion that a certain number of bacterial cells in
the product is necessary and that the bacteria of the
yoghurt culture have a greater lactose-digesting
potential than L. acidoplzillls although strain differences have to be acknowledged (Sanders, 1993).
to
after ingestion of milk, yoghurt, and milk fermented by
S. thermophilus, L. bulgaricus, B. bifidum, and L.
acidophilus (from Martini et al., 1991b).
leche, yogur y leche fermentada con S. thermophilus,
L. bulgaricus, B. bifidum, and L. acidophilus (datos
segun Martini et al., 1991 b).
Heat-treated cultured
(3-galactosidase activity. These products were adto healthy lactose malabsorbers. All
yoghurts dramatically and similarly improved lactose
digestion, as shown by the flat breath H, curve in
Figure 8, regardless of their total or specific (3-galacministered
tosidase activity. However, the response from fermented milk varied from marginal improvement with
B. bifidmu to almost complete lactose digestion ~~ith
L. bulgaricus. The results suggest that total j3-galactosidase was not the limiting factor in promoting
lactose digestion, because of a limited rate of intracelluar substrate transport. From some of these results
it may be concluded that the substrate lactose may
enter the microbial cell, where it is split, and the
break-down products glucose and galactose are
released from the cell.
The favourable effect of the traditional yoghurt
culture is explained by the fact that L. btilgai-icits
and S. therl1loplzilus have higher concentrations of
lactase, that they are bile-sensitive and are therefore
much more suitable for enzyme delivery applications. The strains applied should be permeable so
that lactase can be released from the bacterial cell
(Sanders, 1993).
Non-fermented milk
question of whether non-fermented
taining lactic acid bacteria is also able to
The
milk
con-
contribute
Marteau et nl.
products
(1990) conducted experiments where
the effect of
administering heat-treated cultured dairy
lactose digestion was examined. In these
products
experiments, 18 g of lactose were given to lactase-deficient volunteers in the form of milk, yoghurt and
heated yoghurt. The total excess breath hydrogen was
reduced by 46% after the ingestion of unheated
yoghurt compared to heated yoghurt.
on
Exogenous
lactase
The
related to the effect of exogenous lactdigestion was examined by Onwulata
by administering commercially available
question
ase on
et al.
lactose
(1989)
plain yoghurt, sweet acidophilus milk, lactose-hydrolysed milk, a lactase tablet, and whole milk to
lactose-intolerant black subjects. Each product contained 18 g lactose except the lactose-hydrolysed milk
which had 5 g. From the data shown in Figure 9
the following conclusions can be made: (i) There was
a significant positive correlation between the symptoms reported and the mean peak of breath hydrogen ; (ii) lactose-hydrolysed milk was similar to
yoghurt in its effect in minimizing lactose maldigestion ; (iii) no effect of sweet acidophilus milk could
be seen compared with whole milk; and (iv) the
microbial endogenous lactase in yoghurt is superior
to
exogenous commercial lactase.
77
9. Changes in the breath hydrogen levels of
lactose-intolerant subjects after consuming various milk
products (from Onwulata et al., 1989).
Figure
after ingestion of milk, yoghurt, a standard breakfast
meal, and yoghurt plus the meal (from Martini et al.,
1991a).
Figura 9. Cambios en el hidr6geno eliminado en la
respiraci6n en individuos que no toleran la lactosa
despu6s de consumir diferentes productos 16cteos
(datos segun Onwulata et a/.,1989).
leche, yogur, un desayuno est6ndar, y un yogur m6s el
desayuno (datos segun Martini et al., 1991a).
nothing to the ability to tolerate and digest plain,
full-fat yoghurt, but it may be useful with low-fat or
pasteurized varieties.
Lactose-hydrolyzed yoghurt
Whether prehydrolysis of yoghurt milk may further
contribute to lactose digestion was examined by
Rosado et al. (1992). In this study, three yoghurt products were given to lactose-maldigesters: unmodified
plain yoghurt, low-fat yoghurt, and yoghurt produced from lactose-hydrolysed milk. It could be
observed that intolerance symptoms were significantly and equally reduced with all yoghurt products
compared to milk (although it was found that lactosedigesters had a significantly greater efficiency of
lactose digestion than maldigesters). Furthermore,
as shown in Table 1, lactose prehydrolysis adds
hydrogen excretion and symptoms after
maldigesters (data from Rosado efa/., 1992).
Table 1. Breath
,
Intake of
yoghurt
with
a
rf
meal
ability of yoghurt ~3-galactosidase to digest lactose when yoghurt is consumed
with a meal, Martini et al. (1991a) conducted a study
where healthy lactose-maldigesting individuals were
fed several test meals. The results shown in Figure 10
indicate that the consumption of a meal with yoghurt
does not inhibit, and may slightly improve, lactose
digestion from yoghurt.
In order to evaluate the
the intake of different types of
Tabla 1. Eliminaci6n de hidr6geno en la respiraci6n frente
despu6s de ingerir diferentes tipos de yogur y leche (datos
a
yoghurts
la respuesta de individuos mal
segun Rosado
et
al., 1992).
and milk
digestores
by
lactose
de lactosa,
78
Figure 11. Breath hydrogen concentrations produced
after the ingestion of milk, yoghurt and yoghurt with
additional lactose (from Martini et al., 1991a).
Figura
11. Cambios en la concentraci6n del hidr6geno
en la respiraci6n despu6s de la ingestion de
eliminado
leche, yogur, y yogur con adici6n de lactosa (datos
Martini et al., 1991a).
segun
Additional lactose
The
authors (Martini et al., 1991a) examined the
whether
additional lactose in yoghurt can be
question
too.
digested
They concluded (Figure 11 ) that yoghurt
(3-galactosidase appears unable to assist in the digestion of additional lactose beyond that normally
present in yoghurt. These results have some practical
implications: very often, yoghurt milk is pre-concentrated, therefore, these products have higher lactose
levels; if recombined milk is used for yoghurt manufacture, higher lactose concentrations may be found
in these products too.
same
REFERENCES
Berg A., Eriksson M., Barany F., Einarsson K., Sundgren H.,
Nylander C., Lundstrom Y. and Blomstrand R. (1985).
Hydrogen concentration in expired air analyzed with a
new hydrogen sensor, plasma glucose rise, and symptoms
of lactose intolerance after oral administration of 100 g lactose. Scandinavian Journal of Gastroenterology 20: 814-822.
Brand J.C. and Holt S. (1991). Relative effectiveness of milks
with reduced amounts of lactose in alleviating milk intolerance. American Journal of Clinical Nutrition 54: 148-151.
Brand Miller J.B. and Munro V. (1992). The effectiveness
of 50% lactose-reduced milk in alleviating milk intolerance. Asian Pacific Journal of Clinical Nutrition 1:
245-248.
Cavalli-Sforza L.T., Strata A., Barone A. and Cucurachi L.
(1987). Primary lactose malabsorption in Italy: Regional
differences in prevalence and relationship to lactose intolerance and milk consumption. American Journal of Clinical
Nutrition 45: 748-754.
DiPalma J.A. and Collins M.S. (1989). Enzyme replacement
for lactose malabsorption using a β-D-galactosidase.
Journal of Clinical Gastroenterology 11: 290-293.
Kolars J.C., Levitt M.D., Aouji M. and Savaiano D.A. (1984).
Yogurt - an autodigesting source of lactose. New England
Journal of Medicine 310: 1-3.
Lin M.-Y., Savaiano D. and Harlander S. (1991). Influence of
nonfermented dairy products containing bacterial starter
cultures on lactose maldigestion in humans. Journal of
Dairy Science 74: 87-95.
Lybeck Sörensen K., Vergara Meersohn M., Sonne J., Larsen
L., Edelsten D. and Gudmand-Höyer E. (1983). A new
type of low-lactose milk. Scandinavian Journal of
Gastroenterology 18: 1063-1068.
Marteau P., Flourie B., Pochart P., Chastang C., Desjeux J.F.
and Rambaud J.C. (1990). Effect of the microbial lactase
(EC 3.2.1.23) activity in yoghurt on the intestinal absorption of lactose: an in vivo study in lactase-deficient
humans. British Journal of Nutrition 64: 71-79.
Martini M.C. and Savaiano D.A. (1988). Reduced intolerance
symptoms from lactose consumed during a meal.
American Journal of Clinical Nutrition 47: 57-60.
Martini M.C., Kukielka D. and Savaiano D.A. (1991a).
Lactose digestion from yogurt: influence of a meal
and additional lactose. American Journal of Clinical
Nutrition 53: 1253-1258.
Martini M.C., Lerebours E.C., Lin W. J., Harlander S.K.,
Berrada N.M., Antoine J.M. and Savaiano D.A. (1991b).
Strains and species of lactic acid bacteria in fermented
milks (yogurts): effect on in vivo lactose digestion.
American Journal of Clinical Nutrition 54: 1041-1046.
Onwulata C.I., Rao D.R. and Vankineni P. (1989). Relative
efficiency of yoghurt, sweet acidophilus milk,
hydrolyzed-lactose milk, and a commercial lactase tablet
in alleviating lactose maldigestion. American Journal of
Clinical Nutrition 49: 1233-1237.
Payne D.L., Welsh J.D., Manion C.V., Tsegaye A. and Herd
L.D. (1981). Effectiveness of milk products in dietary
management of lactose malabsorption. American Journal
of Clinical Nutrition 34: 2711-2715.
Renner E. (1983). Milk and dairy products in human nutrition.
München: Volkswirtsch. Verlag.
Renner E. and Renz-Schauen A. (1992). Nutrition composition tables of milk and dairy products. Giessen:
Verlag B. Renner.
Rosado J.L. and Solomons N.W. (1983). Sensitivity and specifity of the hydrogen breath-analysis test for detecting malabsorption of physiological doses of lactose. Clinical
Chemistry 29: 545-548.
Rosado J.L., Solomons N.W. and Allen L.H. (1992). Lactose
digestion from unmodified, low-fat and lactose-
79
hydrolyzed yogurt in adult lactose-maldigesters. European Journal of Clinical Nutrition 46: 61-67.
Saavedra J.M. and Perman J.A. (1989). Current concepts in
lactose malabsorption and lactose intolerance. Annual
Review of Nutrition 9: 475-502.
Sanders M.E. (1993) Summary of conclusions from a consensus panel of experts on health attributes of lactic cultures: significance to fluid milk products containing
cultures. Journal of Dairy Science 76: 1819-1828.
Sategna-Guidetti C., Cruto E. and Capobianco P. (1989)
Breath hydrogen excretion after lactose and whole milk
ingestion. Journal of Clinical Gastroenterology 11: 287-289.
Simoons F.J. (1978). The
A
geographic hypothesis and lactose
weighing of the evidence. American
malabsorption:
Journal of Digestive Diseases 23: 963-980.
Solomons N.W. (1986). An update on lactose
intolerance.
Nutrition News 49
(1): 1-3.
Solomons N.W., Guerrero A.M. and Torun B. (1985).
Effective in vitro hydrolysis of milk lactose by beta-galactosidases in the presence of solid foods. American Journal
of Clinical Nutrition 41: 222-227.

Dietary approaches to alleviation of lactose maldigestion Efectos de

Transcripción

Documentos relacionados

Arroz con leche (rice pudding) Ingredients: 3 liters of regular whole

Developmental Milestones