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TNO Nutrition and Food Research, Nutritional Physiology, Utrechtseweg 48, Zeist, The Netherlands and * Borculo Domo Ingredients, Development and Application, Needseweg 23, Borculo, The Netherlands
2To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • transgalactooligosaccharides • calcium absorption • stable isotopes • postmenopausal women
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Wargowich et al. 1984
). This hypothesis is underscored by the results of
Wijnands et al. (1999)
who reported an inhibitory effect
of TOS on multiplicity and size of colorectal tumors in rats. In
addition, colonic fermentation of TOS can facilitate calcium
absorption. This has been shown in rat experiments (Chonan et al. 1995
, Chonan and Watanuki 1995
and 1996
).
Only one human study has reported the effect of TOS on Ca absorption.
No effect of 15 g NDO, including TOS, on iron or calcium
absorption was found in healthy men (van den Heuvel et al. 1998
). As suggested previously (van den Heuvel et al. 1999a
), the absence of a positive effect in that study was
probably due to the method applied. i.e., dual stable isotope
technique, which may not have included the colonic component of Ca
absorption because the amount of Ca absorbed after 24 h of isotope
administration was not measured. Although data concerning the effect of
other NDO on Ca absorption in humans are scarce, they do underscore the
positive effect found in rats (Coudray et al. 1997
,
van den Heuvel et al. 1999a
and 1999b
). In these
studies, complete Ca absorption was measured, including the colonic
component.
The aim of this study was to investigate whether a product rich in TOS
(Elix'or, Borculo Domo Ingredients, Borculo, The Netherlands)
stimulates true Ca absorption in postmenopausal women, who have a
decreased efficiency of Ca absorption (Heaney et al. 1989
). True Ca absorption was determined with the dual stable
isotope technique by measuring the excretion of Ca isotopes in urine
collected over 36 h after oral and intravenous isotope
administration.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The subjects in this study were recruited from a pool of volunteers
from TNO Nutrition and Food Research Institute and via an advertisement
in the local newspaper and television news. Fourteen women (including
two substitutes) were selected; they reported being postmenopausal for
at least 5 y, which was confirmed by a high level of
follicle-stimulating hormone (FSH; 64–126 U/L, mean
104 U) and a low level of estradiol (E2; from <20 to 43
ng/L). One woman had an E2 concentration >35 ng/L and five had levels
<20 ng/L. At the start of the study, the subjects’ age ranged from 55
to 65 y (mean 62 y); their body weights were from 57.2 to
85.8 kg (mean 73.1 kg) and their body mass indices (BMI) from 20.7 to
32.4 kg/m2 (mean 26.4 kg/m2). Normal health was
assessed at the prestudy screening, which involved physical
examination, medical history, measurement of blood pressure and heart
rate, and routine clinical laboratory tests. On the basis of the third
Dutch National Food Consumption Survey (DNFCS) of 1997 and 1998, which
showed that women aged 50–65 y have a mean fiber intake of 21 g/d
(Centre of Nutrition 1998
), only subjects with a
habitual fiber intake between 18 and 26 g/d (mean 22.3) were selected
on the basis of a food-frequency questionnaire (FFQ). The FFQ was
developed in FOFREX (Food Frequency Expert), a computerized system with
data from the second DNFCS of 1992 (National Education Board 1992
) and a predefined question matrix.
Before the study, subjects were challenged with a single dose of 
10
g of TOS (Elix'or, Borculo Domo Ingredients) dissolved in a yogurt
drink to check for possible intolerance. No signs of intolerance or
intestinal discomfort were reported. None of the subjects were taking
calcium or fiber supplements, were smokers or were taking drugs known
to interfere with calcium metabolism. All reported a typical Dutch food
pattern (National Education Board 1992
) and all reported
consumption of dairy products. All subjects gave informed consent to
participate in the study after procedures had been explained to them.
The study protocol was approved by the TNO external Medical Ethics
Committee.
Study design and execution of the study.
The study was a double-blind, randomized crossover study,
consisting of two 9-d treatment periods separated by a 19-d washout
period. At breakfast and lunch during the treatment periods, the
subjects drank 200 mL of a yogurt drink (213 g) containing either TOS
(Elix'or) or the reference substance, sucrose. A supplement of 20 g TOS to the diet was achieved by using NDO-enriched products and
was expected to be well tolerated. The first symptoms of intolerance
(excessive flatulence) seemed to occur after consumption of >30 g/d of
fructooligosaccharides (Briet et al. 1995
) and after a
single dose of short-chain fructans (DP < 10; median: DP
= 3) and long-chain fructans (DP > 12) of over 20 g
(Rumessen and Gudmand-Høyer 1998
). In this study,
adaptation to the oligosaccharides was ensured by gradually increasing
the daily dose of TOS from 10 g/d (22 g Elix'or) to 20 g/d (44 g
Elix'or) over a period of 5 d (10 g TOS on d 1 and 2, 15 g on
d 3 and 4, 20 g on d 5–9). Thus, 20 g TOS was administered
for only 5 d. Table 1
shows physicochemical properties of the study substance, Elix'or, and
Table 2
shows the composition of the yogurt drinks. All yogurt drinks had the
same taste (peach) and sweetness, as tested by a sensory panel.
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Preparation of stable isotope solutions.
The stable isotopes were obtained from Chemgas (Boulogne, France) in
the form of CaCO3. The abundances of the different Ca
isotopes according to analysis by inductively coupled plasma mass
spectrometry (ICP-MS) were as follows: 3.39% 40Ca, 0.06%
42Ca, 0.03% 43Ca, 96.5% 44Ca,
<0.01% 46Ca, 0.02% 48Ca for Ca enriched in
44Ca, and 2.82% 40Ca, <0.001%
42Ca, 0.007% 43Ca, 0.10% 44Ca,
<0.001% 46Ca, 97.07% 48Ca for Ca enriched in
48Ca. The 44CaCO3 was converted
into chloride salt, diluted with deionized water, followed by pH
adjustment to 5. A similar procedure was followed for
48CaCO3, except that saline was used instead of
deionized water. After filtration, the solution was distributed over
10-mL injection bottles and sterilized for 20 min at 121°C. The
44CaCl2 was added to the yogurt drink in the
morning of the test days 1 h before oral administration.
Stable isotope analysis.
The concentration of Ca in the urine samples was measured by atomic
absorption spectrometry (AAS). 44Ca/43Ca and
48Ca/43Ca isotope ratios in urine were measured
by ICP-MS (VG PlasmaQuad, Fisons Instruments, UK) after
protein precipitation with 3.5% trichloroacetic acid, precipitation of
Ca with saturated ammonium oxalate and dissolution of the formed
calcium oxalate in 1.2 mol/L HCl. The Ca concentration in the HCl
solution was measured by AAS and diluted if necessary to adjust to 1
mg/L Ca. Urine spot samples and 36-h urine samples taken during each
treatment, before and after isotope administration to the same subject,
were measured by ICP-MS within 1 d, together with a blank and
a standard of 1 mg/L Ca. All values were adjusted for minor deviations
from standard Ca solutions with accepted natural ratios. All samples
were measured in duplicate.
Taking into account the amount administered and the natural abundance
of these isotopes, true absorption was calculated from the isotope
ratios in urine collected before dose administration and over the
36 h after dose administration, as reported by Van Dokkum et al. (1996)
.
Statistics.
The data were analyzed by regression analysis for a Latin-square
design (SAS V6.12/V8.0, SAS Institute, Cary, NC). Statistically, the
null hypothesis was that there is no positive effect of TOS consumption
on Ca absorption. Because previous human studies (Coudray et al. 1997
, van den Heuvel et al. 1999a
and 1999b
)
indicated a positive effect of NDO on Ca absorption, the alternative
hypothesis was a positive effect of 20 g TOS/d on Ca absorption.
The null hypothesis was to be rejected at P < 0.05
(one-sided). Regression analysis was used to assess associations
between variables.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Compliance as checked by returned yogurt drinks and questionnaires was 100%. No adverse side effects (gastrointestinal complaints or changes in stools) were seen after intake of 20 g TOS compared with the control treatment.
All samples were measured in duplicate. Within-duplicate variation (CV) was 0.72% for the 44Ca/43Ca ratio and 0.91% for the 48Ca/43Ca ratio.
It was not possible to measure the basal urine sample of one subject for each treatment period due to a small amount of Ca in the urine. The basal ratios were replaced in these cases by the average of basal 44Ca/43Ca and 48Ca/43Ca ratios per treatment period. The average basal 44Ca/43Ca ratio was 15.431 (CV 0.98%) and the 48Ca/43Ca ratio was 1.380 (CV 1.05%). The average enrichment value (mean ± SEM; n = 23) was 3.30 ± 0.21% for the urinary 44Ca/43Ca ratio and 12.58 ± 0.42% for the urinary 48Ca/43Ca ratio.
Table 3
shows the mean basal and enriched
44Ca/43Ca and
48Ca/43Ca ratios and the
enrichment percentages of these ratios per treatment. No significant
differences were found between treatments. Ca absorption (mean ± SEM) was 23.9 ± 6.9% during the treatment with TOS
(n = 11) and 20.6 ± 7.0% during the reference
treatment (n = 12) (P = 0.04,
one-sided). A relative increase in Ca absorption by 16% was found
[standard error of the difference (SED) = 5.76].
Figure 1
shows the mean and individual differences in Ca absorption. Even
excluding the woman who showed the highest TOS-induced increase in
Ca absorption (see Fig. 1
), the difference was significant
(SED = 3.01; P = 0.02, one- sided).
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0.05). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) exists that is nearly
comparable to the present study. In that study, in postmenopausal women
with an unknown fiber intake, relative increases in Ca absorption of 8
and 16% were found as a result of a daily intake of a single dose of 5
or 10 g, respectively, of lactulose during breakfast. This
breakfast provided a smaller amount of calcium (162 mg) than the
breakfast given in the present study (250 mg). In the present study,
the dose of TOS was divided between breakfast and lunch, and a 16%
increase in Ca absorption was found. We assumed that TOS given during
lunch would still exert an effect on the absorption of Ca from
breakfast, which was enriched with stable isotopes. However, there are
indications that the increase in Ca absorption was due solely to the
10 g of TOS taken during breakfast. In rats, the direct and
indirect effects on Ca absorption of another nondigestible carbohydrate
were studied by feeding lactulose either before or after the test meal
containing 47Ca. From the results, it was
concluded that lactulose must be present in the meal in order to
observe its stimulant effect (Brommage et al. 1993
).
This may suggest that the increase in Ca absorption found in the
present study was due to the 10 g TOS present in the breakfast
containing the stable isotope. The acute positive effect of lactulose
was nonspecific and shared, at least in rats, by other NDO
(Brommage et al. 1993
). Whether this is also the case in
humans should be confirmed by further research because the studies on
lactulose and TOS involved two different human studies.
Intestinal calcium absorption proceeds by two mechanisms, an active
transcellular process and a passive paracellular process
(Bronner 1998
). Both transport mechanisms may be
affected by NDO in several ways, i.e., hypertrophy of the cecal wall
and a greater surface area, an increase in soluble calcium due to
fermentation and an accelerated blood flow (Chonan and Watanuki 1995
, Younes et al. 1996
). In addition to these
causal factors, it has been hypothesized that NDO stimulate
transcellular Ca absorption by a direct effect of the SCFA produced.
The direct effect of SCFA probably involves an exchange of
intracellular H+ for Ca2+
present in the distal colon (Lutz et al. 1991
,
Trinidad et al. 1996
). The rate-limiting step in
transcellular calcium movement is, however, the diffusion of
Ca2+ across the cytoplasm. Calbindin plays an
important role in the intracellular diffusion rate of the calcium ion
(Bronner 1998
). In gastrectomized rats fed
fructooligosaccharides, the amount of calbindin was increased in both
cecal and colorectal segments and decreased in the proximal and distal
small intestine. The overall effect, however, was an improved Ca
absorption due to NDO (Ohta et al. 1998
). Future work
should address the mechanism by which ingestion of NDO improves mineral
absorption.
In addition to TOS, the study substance contained lactose, which is
another nutrient that may increase Ca absorption under certain
conditions. In this study, the increase in Ca absorption was probably
due solely to TOS. In rats, lactose vs. glucose caused an increment in
mean Ca absorption, but this effect failed to reach significance
(Heijnen et al. 1993
). Others have also found that
lactose does not induce increases in Ca absorption (Armbrecht and Wasserman 1976
, Chonan et al. 1995
,
Favus and Angeid-Backmann 1984
). Rats become lactase
deficient after weaning (de Groot et al. 1957
) and hence
are not capable of hydrolyzing lactose in the intestine. Possibly,
fermentation of lactose in the intestine may increase the solubility of
intestinal Ca, leading to increased absorption. Although lactose seems
to increase Ca absorption in lactase-deficient infants
(Saarela et al. 1995
), no effect of lactose on Ca
absorption has been found in premature children (Stathos et al. 1996
), premenopausal women (Nickel et al. 1996
)
or adult volunteers (Brink et al. 1993
). Taking into
account the data from the literature, no effect of lactose on Ca
absorption in healthy, lactose-tolerant people is to be expected.
This is underscored by the results of Zitterman et al. (2000)
. In addition, Chonan et al. (1995)
found
in 4-wk old male rats a dose-dependent increase of calcium
absorption due to TOS, but not due to lactose. Together with the higher
percentage of TOS in the study substance, this may indicate that the
increase of Ca absorption in the present study is likely due solely to
the TOS present in the study substance.
According to Bronner and Pansu (1999)
, probably no
> 10% of total calcium absorption takes place in the large
intestine. However, when acidic fermentation of TOS takes place, the
large intestine may represent a major site of Ca and Mg absorption
(Younes et al. 1996
). This may be of particular
importance when the overall process of digestive absorption is
inefficient, such as in elderly subjects (Andon et al. 1993
). Over a 20-y period of observation, aging and estrogen
decline produce a 20–25% deterioration in absorptive performance from
age 40 to 60 y (Heaney et al. 1989
). The results of
the present study demonstrate that TOS may help correct for this
decrease in absorption capacity, without increasing urinary Ca
excretion. Animal studies support this finding (Chonan et al. 1995
, Chonan and Watanuki 1995
and 1996
). In two
rat studies, calcium balance was examined together with bone
mineralization (Chonan et al. 1995
, Chonan and Watanuki 1996
). The results indicated that the increased
calcium absorption produced by TOS coincided with an elevation of the
Ca content of bone.
In conclusion, in this study in postmenopausal women, an increased Ca absorption was observed after consumption of a product rich in TOS (Elix'or) compared with the reference treatment. This increase in Ca absorption was probably due solely to the TOS. The increased Ca absorption was not accompanied by increased urinary Ca excretion, implying that TOS also may increase the uptake of Ca by the bones and/or inhibit bone resorption. More research is required to explore whether TOS is able to improve Ca balance in humans and/or reduce the prevalence of osteoporosis.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: AAS, atomic absorption
spectrometry; DNFCS, Dutch National Food Consumption Survey; DP, degree
of polymerization; E2, estradiol; FFQ, food-frequency
questionnaire; FSH, follicle-stimulating hormone; ICP-MS,
inductively coupled plasma mass spectrometry; NDO, nondigestible
oligosaccharides; SCFA, short-chain fatty acids; TOS,
transgalactooligosaccharides.
Manuscript received June 2, 2000. Initial review completed June 30, 2000. Revision accepted August 25, 2000.
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