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Journal of the American College of Nutrition, Vol. 24, No. 1, 30-37 (2005)
Published by the American College of Nutrition

Influence of Short-Chain Fructo-Oligosaccharides (sc-FOS) on Absorption of Cu, Zn, and Se in Healthy Postmenopausal Women

Véronique Ducros, PhD, Josiane Arnaud, PhD, Maha Tahiri, PhD, Charles Coudray, PhD, Francis Bornet, PhD, MD, Corinne Bouteloup-Demange, PhD, MD, Fred Brouns, PhD, Yves Rayssiguier, PhD, FACN and Anne Marie Roussel, PhD, FACN

Laboratoire Nutrition, Vieillissement et Maladies Cardiovasculaires, Université Joseph Fourier, Domaine de la Merci, 38700 La Tronche (V.D., J.A., A.M.R.)
Département de Biologie Intégrée, Centre Hospitalier Universitaire, BP 217, 38043 Grenoble cedex 9 (V.D., J.A.)
Centre de Recherche en Nutrition Humaine d’Auvergne, Unité Maladies Métaboliques et Micronutriments, Centre de Recherche INRA Clermont-Ferrand/Theix, 63122 Saint Genès Champanelle (M.T., C.C., Y.R.)
Nutrihealth SA, 3 Avenue Paul Doumer, Rueil Malmaison, Paris (F.Bo)
Laboratoire de Nutrition Humaine, 58 rue Montalembert, 63009 Clermont-Ferrand (C.B.-D.), FRANCE
Cerestar R&D Center, Vilvoorde, Belgium, Nutrition & Toxicology Research Institute, Department of Human Biology, Maastricht University, Maastricht (F.Br), THE NETHERLANDS

Address reprint requests to: Véronique Ducros, PhD, Département de Biologie Intégrée, Centre Hospitalier Universitaire, BP 217, 38043 Grenoble cedex 9, France. E-mail: VDucros@chu-grenoble.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Objective: This study was carried out to evaluate the effect of short-chain fructooligosaccharides (sc-FOS) on the absorption of Cu, Zn, and Se among postmenopausal women who are potential candidates to subclinical trace element deficiencies.

Design: A randomized double blind cross-over study.

Setting: This study was carried out at the Human Nutrition Research Center, Clermont-Ferrand, France.

Subjects: 11 postmenopausal women aged 53–70 y, not taking hormone replacement therapy were enrolled and completed the study.

Interventions: Diets with 10 g/day sc-FOS or placebo were given for 5 weeks each in random order followed by a wash-out period of at least 3 weeks. At the end of each period, stable isotopes (3.19 mg 67Zn as ZnCl2, 2.06 mg 65Cu as CuCl2 and 52.3 µg 74Se as sodium selenite) and radiopaque pellets (as fecal excretion index) were administered during lunch. Stools were collected for the next 5–7 days. Isotopes were determined by ICP-MS (Cu and Zn) or GC-MS (Se).

Results: Copper absorption was significantly enhanced (p = 0.042) by sc-FOS. No effect of sc-FOS was observed on Zn, and Se absorption.

Conclusion: To our knowledge, this is the first study on the influence of sc-FOS on trace element metabolism. The observed increase in copper absorption may be of interest regarding daily copper requirements in menopausal women. However, the relevance of this observation remains to be established.

Key words: fructo-oligosaccharides, absorption, trace elements, postmenopausal women, stable isotopes

Abbreviations: HRT = hormone replacement therapy • GC-MS = gas chromatography-mass spectrometry • ICPMS = inductively coupled plasma mass spectrometry • IR = isotopic ratio • NDOs = nondigestible oligosaccharides • sc-FOS = short-chain fructooligosaccharides


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Cardiovascular diseases and osteoporosis increase considerably in postmenopausal women [1,2]. Marginal status in minerals and trace elements have been both considered as a risk factor for osteoporosis (Ca, Mg, Cu, Zn) [3] and for cardiovascular diseases (Mg, Cu, Zn, Se) [4]. In particular, the potential benefits of Cu and Zn supplementation in reducing bone loss in postmenopausal women has been observed [5,6]. Some studies have reported that the maintenance of an optimal Se status protects elderly against reduced peripheral conversion of thyroxine to tri-iodothyronine [7], cognitive decline [8], cardiovascular diseases and cancers [9] due to its antioxidant properties. In developed countries, female population is becoming older and from a public health point of view, it is interesting to evaluate new sources of products able to increase mineral or trace element status by different ways including the enhancement of mineral or trace element absorption. Short-chain fructo-oligosaccharides (sc-FOS), known as prebiotics, consist of glucose linked to two, three, or four fructose units. Links between fructose units are of ß-(2-1) type. Basically FOS are not absorbed in the small intestine, and are completely fermented by colonic flora [10]. FOS have been proven to enhance intestinal absorption of Ca, Mg, Fe, Zn and Cu in rats [11–14]. The effects of FOS on Ca, Mg and Fe absorption in humans are less clear. Some human studies showed a positive effect on Ca absorption [15,16] or Mg absorption [17] whereas one showed no effect on Ca and Fe absorption [18] but the authors mentioned that this absence of any effect on Ca absorption might be due to methodological problems [18]. However less attention has been paid on Cu, Zn, and Se absorption under FOS administration. This study was part of a larger one aiming to measure the impact of moderate daily doses of sc-FOS ingestion on minerals (Ca, Mg) and trace element (Cu, Zn, Se) absorption in postmenopausal women. Results on Ca and Mg bioavailability and status have already been published [16,17]. The present paper is therefore focused on Cu, Zn, and Se absorption.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Reagents
Two mg of enriched 74Se (99.99%) stable isotope in the metal form; 96 mg of enriched 67Zn (93.3%) stable isotope in the oxide form, and 70 mg of enriched 65Cu (99.2%) stable isotope in the metal form, were obtained from Chemgas (Paris, France). Enriched 82Se (96.7%) stable isotope was previously purchased from the Oak Ridge Laboratory (Oak Ridge, TN) also as metal powder for use as internal standard in isotopic dilution analysis. Suprapure 65% HNO3, 30% H2O2, 30% HCl, 1 M NaOH and Se, Zn and Cu (1 g/L) standard solutions were obtained from Merck (Darmstadt, Germany). All other chemicals were of the highest quality available. Demineralized water was obtained from an Elga apparatus (Elga, Villeurbanne, France).

Treatments
Actilight® (Eridania Béghin-Say, Neuilly Sur Seine, France) is a mixture of short chain fructo-oligosaccharides (sc-FOS), produced by enzymatic treatment of sucrose with fungal transfructosylase. The main composition of the obtained sc-FOS is as follows: 37% of 1-kestose (one sucrose molecule plus one fructose molecule), 53% of nystose (one sucrose molecule plus two fructose molecules), and 10% of fructosyl-nystose (one sucrose molecule plus three fructose molecules). The placebo consisted of sucrose.

Preparation of the Stable Isotope Solution
The isotope method used was an extrinsic multiple labeling consisting of a combined oral dose of 25Mg, 44Ca, 67Zn, 65Cu and 74Se. Concentrated HCl was used to transform oxide (Zn) or metal (Cu) into chloride forms. Sodium selenite was prepared by oxidizing metal 74Se in suprapure 65% HNO3 to obtain Se dioxide (SeO2) and further by adding 1 N NaOH to transform SeO2 into sodium selenite. The final pH of the stable isotope mixture was adjusted to 2 with 1 N NaOH. The concentration of total Zn, Cu, and Se as well as isotopic enrichment of the mixture were checked before used. Total 67Zn, 65Cu, and 74Se amount in administered dose were 3.19 mg, 2.06 mg, and 52.3 µg respectively. The final solution was controlled for abnormal toxicity on mice (CERB, Baugy, France) and for the pharmaceutical conformity form for human use (Clermont-Ferrand University Hospital pharmacy, France).

Subjects
14 healthy postmenopausal women were recruited: age between 50–70 years with at least 2 years of menopause, no HRT, no intake of nutritional supplements containing vitamins, minerals, polyols, fibre, and FOS during the study length as well as the 3 months prior to the study, and a body mass index between 20–27 kg/m2. Exclusion criteria were digestive, hepatic, renal, or inflammatory diseases, any surgery for three months before the study, drugs interfering with absorption like antibiotics and laxatives, and vegetarian diets which have a high content in fermentable fibre. Before the interventional study, the food consumption habit of the volunteers was assessed by a food frequency questionnaire for six months prior to the start of the study. Health state was assessed by a medical history, physical examination, and routine clinical laboratory tests. The volunteers were fully informed of the aim and purpose of the study, and signed an informed consent. The protocol of this study, registered under the reference AU260, was approved by the local ethical committee of the Human Nutrition Research Center at Clermont-Ferrand (France).

Study Design
A double blind cross-over study was designed with postmenopausal women acting as their own controls (Fig. 1). Nutritional supplements containing sc-FOS or placebo having an identical taste were ingested for a period of 35 days, in random order. Between these periods, there was a wash-out period of at least 3 weeks. Compliance was followed by asking volunteers to bring back the unused supplements at the half-way and end of each period.



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  		Fig. 1. Schema of the study design. A double blind cross-over study with postmenopausal women acting as their own controls.

 
Volunteers received 5 g of sc-FOS per day for the first 4 days only at lunch and then 10 g/day (5 g at lunch and 5 g at dinner) to allow for adaptation. During the first 23 days, volunteers were asked to maintain their normal food intake. They were not allowed to eat oligosaccharide-containing food products or mineral or vitamin supplements. Daily balanced low-dietary fiber menus were offered to volunteers from the 5th day before the isotope administration to the 5–7th day after the stable isotope administration as previously described [16,17]. A set of 4 day menus was prepared and repeated all along the controlled diet period. Volunteers were instructed to avoid additional food, particularly snacks, and to bring back the leftovers on the next day in order to evaluate their trace element intake.

On day 28, volunteers received the combined enriched stable isotope dose diluted in 100 mL of commercialized Volvic® aromatized water and 40 radiopaque pellets as fecal marker during lunch. The "stable isotope" glass was rinsed twice with about 50 ml of aromatized water.

Blood Sampling and Analysis
Blood sampling was done at inclusion between one to three weeks before the start of the interventional study. Blood samples were collected for total plasma Zn, Cu, and Se determination in trace element free tubes (Vacutainer 7 mL, Becton Dickinson, Pont de Claix, France). Samples were collected after an overnight fasting. After centrifugation, plasma samples were rapidly separated and frozen at –20°C until analyses.

Total plasma Zn was measured by flame atomic absorption spectrometry (Perkin Elmer Model 560, Perkin Elmer, Norwalk, CT) after a five fold dilution in 0.1 M HCl. Total Cu in plasma was measured by flame atomic absorption spectrometry (Perkin Elmer Model 560) after a five fold dilution in 6% n-butanol (v/v). Total plasma Se was measured by GC-MS as previously described [19,20]. Appropriate quality controls (Seronorm serum, Nycomed, Oslo, Norway) were run with each set of measurements. The analyzed Cu, Zn and Se concentration of the quality control (n = 12) were 19.7 ± 0.3 µmol/L, 22.3 ± 0.4 µmol/L and 1.00 ± 0.12 µmol/L compared to certified values of 19.8 ± 1.2 µmol/L, 22.9 ± 1.8 µmol/L and 1.10 ± 0.17 µmol/L, respectively.

Food Collection and Analysis
Controlled menus and leftovers were collected in order to measure Zn, Cu, and Se content for each period and for each subject. Food sample treatments were adapted from previously described methods involving duplicate diet method [21,22]. The food samples were weighted and frozen at –20°C immediately after collection. Later, the frozen samples were thawed, homogenized and frozen at –20°C in a clean room using trace element free material. Then, the samples were freeze-dried by Lyophal (Salon de Provence, France) according to our recommendations to avoid mineral and trace element contamination.

All the determinations were performed in duplicate (Se with imprecision <6%) or in triplicate (Cu with imprecision <5%; Zn with imprecision <3%). All the samples of one subject was treated in the same set of measurements. Appropriate reference material (Total diet, ARC/CL, Jokioinen, Finland) were run with each set of measurements. The analyzed Cu, Zn and Se concentration of the reference material (n = 12) were 3.17 ± 0.09 µg/g, 28.5 ± 0.9 µg/g and 177 ± 11 ng/g compared to certified values of 3.18 ± 0.19 µg/g, 28.9 ± 1.3 µg/g and 181 ± 17 ng/g, respectively.

Fecal Collection
Fecal collections started immediately after the intake of the stable isotopes and lasted 5–7 days. All feces were weighed, X-rayed to count the recovered radiopaque pellets, pooled and homogenized thoroughly. Subsequently, the samples were freeze-dried and the dry weight was determined. The percentage of the recovered pellets was used to ensure the completeness of fecal collection.

Stable Isotope Analysis in Fecal Samples
Feces sample preparation was performed in a clean room. Fecal (0.25 g) samples were first dry ashed and then completely digested with HNO3 and H2O2. The following 65Cu/63Cu, 67Zn/68Zn isotope ratios (IR) were determined in feces collected after the stable isotope administration by using an ICPMS instrument (Plasmaquad PQ2+, ThermoOptek, Les Ulis, France). Blank (0.16N HNO3), samples and standards were acquired five times; zinc and copper ICP/DCP standard solutions (Johnson Matthey, Roissy, France) were used to correct for instrument mass bias. The relative standard deviation for the 65Cu/63Cu, 67Zn/68Zn isotope ratios were <3% and <1% respectively. The 74Se/82Se and 80Se/82Se IR were determined in feces samples; 82Se was used as internal standard. The preparation of the samples, the GC-MS operating conditions as well as the calculations have been previously described in details [19,23]. The relative standard deviation for the 80Se/82Se isotope ratio was <5%.

Calculations
Zn, Cu or Se absorption (%) was calculated as follows = 100 x (administered isotope amount – nonabsorbed isotopes corrected for fecal marker)/(administered isotope amount)

"Nonabsorbed isotopes" corrected for fecal marker excretion was obtained as following: (nonabsorbed isotope x number of excreted pellets)/number of total ingested pellets

Statistics
Results are expressed as means ± SDs. Since it is a cross-over study, a repeated measure ANOVA examining treatment order was first used. If interaction was found, then a PLSD Fisher test was used to check the influence of treatment order and sc-FOS. Statistical analyses were performed using Statview software, version 5 (SAS Institute, Cary, NC, USA). A statistical difference was considered significant when p < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Subject Characteristics and Compliance
Only 11 subjects completed the study. Two were excluded because they needed an antibiotic treatment during the second period of the test. The third one was excluded because feces collection was not complete under the sc-FOS period. The main characteristics of the subjects are reported in Table 1. Based on plasma levels, trace element status of the group was adequate. Compliance and tolerance to the placebo or sc-FOS intakes were considered to be very good: we measured a consumption of 9.79 ± 0.19 g/d for sucrose and 9.83 ± 0.20 g/d for sc-FOS.


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  		Table 1. Main Characteristics of the Subjects and their Plasma Trace Element Concentrations at Inclusion

 
Cu, Zn, and Se Dietary Intakes During the Controlled Diet Period
The proposed Cu, Zn, and Se intakes during the controlled diet periods and the true daily intakes of Cu, Zn, and Se during the same periods were indicated in Table 2. Both results are similar indicating a good compliance to the 4 day menus.


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  		Table 2. Measured Controlled and True Dietary Intakes of Cu, Zn, and Se (Expressed as Mean ± SD, n = 11) and French Recommendations

 
Feces Excretion and Intestinal 65Cu, 67Zn, and 74Se Absorption
Pellet recovery in the collected feces varied between 95 to 100% for the placebo period and between 92.5 to 100% for the sc-FOS period. The fecal excretion mass was significantly different both in wet (83.6 ± 28.0 g/day vs. 119.1 ± 39.1 g/day) and dry (18.5 ± 4.4 g/day vs. 24.1 ± 5.3 g/day) weights, for placebo and sc-FOS periods respectively. In Fig. 2, mean and SD of the Cu, Zn, and Se absorption coefficients for the two treatment periods are indicated as well as the results of the repeated measure ANOVA graphically. For Cu absorption, no interaction between the treatment order and the tested product was observed (p = 0.099, F = 3.39); no effect of the treatment order was noted (p = 0.101, F = 3.33) and interestingly, there is a significant increased in Cu intestinal absorption under sc-FOS period (p = 0.0418, F = 5.62). For Zn absorption, no interaction between the treatment order and the tested product was observed (p = 0.453, F = 0.61); a significant effect of the treatment order (p = 0.039, F = 5.815) was shown but no modification of Zn intestinal absorption coefficient after sc-FOS ingestion (p = 0.383, F = 0.84). For Se absorption, a strong interaction (p = 0.007, F = 11.83) was noted between the treatment order and the tested product (Fig. 1c) but PLSD Fisher test (p > 0.05) showed a lack of effect of the treatment order (p = 0.772, F = 0.09) and of sc-FOS ingestion (p = 0.233, F = 1.64) obtained by repeated measure ANOVA.



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  		Fig. 2. Mean and SD of (a) Cu, (b) Zn, and (c) Se absorption coefficients under placebo or sc-FOS. Interactions are shown graphically.

 

   DISCUSSION
 
Based on previous human studies concerning trace element absorption measurement by using stable isotopes, a number of 12 subjects should be considered adequate [18,24,25]. The potential beneficial effects of fermentable carbohydrates on intestinal mineral and trace element absorption have been extensively investigated in animals [11,12,14,26,27]. However in humans, studies are difficult to perform because of the different volunteers characteristics (age and physiological status), foregoing diets (element intakes/status) and different faecal retention times which all may influence the final result [28,29].

In this study, moderate doses of sc-FOS (10 g/d) were administrated during 5 weeks. This intake is considered to be beneficial for health due to a prebiotic activity [30] and without any side effects [31].

Trace Element Intake
Dietary Cu intake is in the lower range of previous international studies whereas dietary Se and Zn intakes are in agreement with values previously reported in Europe for postmenopausal women [22,32]. However, the measured dietary intake of Zn is very low compared to French dietary recommendation for this age group, ie 10–11 mg/day [33]. Besides the adverse effect of oestrogen deprivation on copper status, low Cu intake in postmenopausal women has been reported [5,6]. The latter may aggravate Cu deficiency in postmenopausal women. The hypothesis that a mild dietary copper deficiency may be implicated in the onset and progression of osteoporosis is also consistent with the literature [34,35].

Trace Element Absorption
Absorption coefficients for Zn, Cu, and Se measured in this study are in agreement with foregoing studies. For Zn, the mean coefficients varying from 24.3% to 30.6% are in agreement with those observed by others (35 ± 10.9% for elderly people [36]) (26%–33% [37]). The mean absorption coefficients of Cu found in our study (from 21.7% to 29.5%) are also similar to those previously reported (26%, 28% and 33.5%) [38–40] using the same technique of fecal monitoring after ingestion of an oral dose of 65Cu. The mean absorption coefficients of Se are lower (from 26.3% to 35.3%) than the expected normal range for selenite (60 to 80%) but are consistent with the result of a previous study [41] where extrinsically labeled selenite was given during lunch and not at fast [41]. With intrinsic labeling, the mean absorption coefficient of Se was similar with and without food [41]. So extrinsic labeling is not the best way to measure bioavailability of Se from foods but intrinsic labeling is very cumbersome and just allows to test one food after another. However in a cross-over study, extrinsic labeling may be enough to check the effect of a treatment on Se absorption under the same conditions of meal.

Indeed the ratio between the isotope dose and the dietary intake, as well as the administration of interactive trace elements such as zinc and copper at the absorption level [42] may contribute to the different influence of sc-FOS on the 3 studied trace element absorption. In this study, the copper stable isotope administration corresponded to more than twice the measured daily dietary copper intake. For zinc, the isotope amount is less than half the measured daily dietary zinc intake. For selenium, the isotope administration is closed to the measured daily dietary selenium intake. However these interactions should affect the results of the sc-FOS and of the sucrose treatment in the same manner.

No effect of sc-FOS intake was observed in this study on Zn absorption in postmenopausal women. Theoretically, Zn absorption is possible in the colon but is low and contribute to Zn absorption only when small intestinal absorption is impaired; that has been shown in rats [43] and in humans [44]. In the same way, no enhancement of Zn absorption has been noted with inulin treatment in young healthy male students [45]. In our group of postmenopausal women, intestinal Zn absorption coefficient was quite normal suggesting that intestinal absorption is not impaired. In the present study, an effect of treatment order is noted for Zn which may indicate that the wash-out period was too short.

A positive effect of sc-FOS intake on Cu absorption was observed. Copper, as well as zinc are generally absorbed from the small intestine. To the contrary of zinc, we have no knowledge of previous experiments showing a possible copper absorption from the colon. One possible explanation for the observed increase in Cu absorption under sc-FOS intake may be a reduction in pH which is assumed to be favorable for Cu absorption in rats [46]. Indeed fermentable carbohydrates such as sc-FOS are known to induce, by acidic fermentation, a decrease in pH in the large bowel [47]. Moreover, the decrease in oestrogenic status after menopause, which emphasizes copper deficiency [34], may facilitate this compensatory mechanism. Our results show for the first time that Cu absorption may be enhanced by sc-FOS supplementation. Sc-FOS by increasing copper absorption may contribute to improve copper status in post menopausal women and help prevent osteoporosis or cardiovascular events. However these preliminary results need to be confirmed.

No effect of sc-FOS intake was also observed for Se absorption. However a strong interaction between the treatment order and the tested product was noted for this trace element. No clear explanation was found to interpret this interaction.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 CONCLUSION
ACKNOWLEDGMENTS
 REFERENCES
 
In this study, the sc-FOS intake has shown an increase in copper absorption but did not exert an effect on zinc and selenium. These data need to be confirmed testing each trace element separately and using more subjects before recommendations can be made.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
REFERENCES
 
The authors are grateful for the technical assistance of Elisabeth Millou (sample preparation), Nicole Belin (GC-MS determination), Laurence Puillet (ICP-MS determination), Jérxome Eudeline and Sandrine Chenal (food sample preparation and AAS determinations). The French Ministry of National Education and Scientific Research and Technology provided financial support for this study (98 G-0069).

Received September 16, 2003. Accepted June 8, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 

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C. Coudray, C. Feillet-Coudray, E. Gueux, A. Mazur, and Y. Rayssiguier
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