Skip to main content

Advertisement

SpringerLink
Log in

Effect of a combination GOS/FOS® prebiotic mixture and interaction with calcium intake on mineral absorption and bone parameters in growing rats

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Aim

Increasing calcium intake is the most effective strategy for avoiding Ca deficit. However, if intake remains inadequate, improving Ca absorption becomes an important tool to optimize Ca homeostasis and bone health.

Purpose

The effect of a mixture of GOS/FOS® 9:1 added to a normal- or low-Ca diets on Ca absorption and bone mineralization, density and structure was investigated, in a model of growing rats. Several colonic parameters to help support the findings were also evaluated.

Results

Weanling Wistar rats received one of the four experimental AIN-93G diets: C5: 0.5 % Ca; C3: 0.3 % Ca; P5: 0.5 % Ca + 5.3 % GOS/FOS®; P3: 0.3 % Ca + 5.3 % GOS/FOS® until 50 days (T = 50). At T = 50, lactobacillus and cecum weights were higher, whereas cecum pH was lower in P5 and P3 versus C5 and C3 (p < 0.001). At T = 50, fecal Ca, Mg and P were lower and their absorptions (mg/dL) were higher in P5 and P3 versus C5 and C3, respectively (p < 0.05). Ca, Mg and P absorption % was higher in P5 and P3 versus C5 and C3 (p < 0.001). Femur Ca and P content, bone mineral content, trabecular bone mineral density, tibia length, bone volume, osteoblast surface, stiffness and elastic modulus were higher in P5 and P3 versus C5 and C3 (p < 0.05). Despite the lower Ca content, P3 group reached similar values than C5 in all these latter parameters.

Conclusions

Supplementing diets with the GOS/FOS® mixture increased bone mineralization, density and structure due to an increase in Ca, P and Mg absorptions. Thus, this prebiotic mixture may help to improve bone development in a period of high calcium requirements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

Ab %:

Absorption percentage

Ab:

Absorption

AIN:

American Institute of Nutrition

BAP:

Bone alkaline phosphatase

BL:

Body length

BV/TV:

Bone volume

BW:

Body weight

Ca:

Calcium

CaI:

Calcium intake

CFU:

Numbers of colony-forming units

DXA:

Dual energy X-ray absorptiometry

ENNyS:

National nutrition and health survey

F:

Feces

FOS:

Fructo-oligosaccharides

GOS:

Galacto-oligosaccharides

GPC.Th:

Whole thickness of the growth plate cartilage

HpZ.Th:

Hypertrophic zone thickness

LS:

Colonies of lactobacillus

Mg:

Magnesium

NDO:

Non-digestible oligosaccharides

P:

Phosphorous

PTH:

Parathyroid hormone

SCFAs:

Short-chain fatty acids

TL:

Tail length

tsBMC:

Total skeleton bone mineral content

tsBMD:

Total skeleton bone mineral density

References

  1. Schettler AE, Gustafson EM (2004) Osteoporosis prevention starts in adolescence. J Am Acad Nurse Pract 16:274–282

    Article  Google Scholar 

  2. Nicklas TA, O’Neil CE, Fulgoni VL (2009) The role of dairy in meeting the recommendations for shortfall nutrients in the American diet. J Am Coll Nutr 28:73S–81S

    Article  CAS  Google Scholar 

  3. Bailey RL, Dodd KW, Goldman JA, Gahche JJ, Dwyer JT, Moshfegh AJ, Sempos CT, Picciano MF (2010) Estimation of total usual calcium and vitamin D intakes in the United States. J Nutr 140:817–822

    Article  CAS  Google Scholar 

  4. Ministerio de Salud (2010) La alimentación de los niños menores de dos años. Resultados de la Encuesta Nacional de Nutrición y Salud -ENNyS 2010, M.d. Salud (ed) Ministerio de Salud Buenos Aires, Argentina, pp 1–60

  5. Kogan L, Abeya-Gilardon E, Mangiolavori G, Biblieri A, Zeni SN (2009) Calcium intake and its relationship to overweight and obesity. Data obtained from the National Survey of Nutrition and Health (ENNyS). Bone 45:S150

    Article  Google Scholar 

  6. Forshee RA, Anderson PA, Storey ML (2006) Changes in calcium intake and association with beverage consumption and demographics: comparing data from CSFII 1994–1996, 1998 and NHANES 1999–2002. J Am Coll Nutr 25:108–116

    Article  CAS  Google Scholar 

  7. Greer FR, Krebs NF, Nutrition AAoPCo (2006) Nutrition, optimizing bone health and calcium intakes of infants, children, and adolescents. Pediatrics 117:578–585

    Article  Google Scholar 

  8. Younes H, Demigné C, Rémésy C (1996) Acidic fermentation in the caecum increases absorption of calcium and magnesium in the large intestine of the rat. Br J Nutr 75:301–314

    Article  CAS  Google Scholar 

  9. Cummings JH, Macfarlane GT (2002) Gastrointestinal effects of prebiotics. Br J Nutr 87:S145–S151

    Article  CAS  Google Scholar 

  10. Molis C, Flourie B, Ouarne F, Gailing MF, Lartigue S, Guibert A, Bornet F, Galmiche JP (1996) Digestion, excretion, and energy value of fructooligosaccharides in healthy humans. Am J Clin Nutr 64:324–328

    CAS  Google Scholar 

  11. Macfarlane S, Macfarlane GT, Cummings JH (2006) Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther 24:701–714

    Article  CAS  Google Scholar 

  12. Pérez-Conesa D, López G, Abellán P, Ros G (2006) Bioavailability of calcium, magnesium and phosphorus in rats fed probiotic, prebiotic and synbiotic powder follow-up infant formulas and their effect on physiological and nutritional parameters. J Sci Food Agric 86:2327–2336

    Article  Google Scholar 

  13. Wang Y, Zeng T, Wang SE, Wang W, Wang Q, Yu HX (2010) Fructo-oligosaccharides enhance the mineral absorption and counteract the adverse effects of phytic acid in mice. Nutrition 26:305–311

    Article  Google Scholar 

  14. Weaver CM, Martin BR, Nakatsu CH, Armstrong AP, Clavijo A, McCabe LD, McCabe GP, Duignan S, Schoterman MH, van den Heuvel EG (2011) Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation. J Agric Food Chem 59:6501–6510

    Article  CAS  Google Scholar 

  15. Scholz-Ahrens KE, Ade P, Marten B, Weber P, Timm W, Acil Y, Gluer CC, Schrezenmeir J (2007) Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr 137:838S–846S

    CAS  Google Scholar 

  16. Boehm G, Fanaro S, Jelinek J, Stahl B, Marini A (2003) Prebiotic concept for infant nutrition. Acta Paediatr Suppl 91:64–67

    CAS  Google Scholar 

  17. Westerbeek EA, Slump RA, Lafeber HN, Knol J, Georgi G, Fetter WP, van Elburg RM (2013) The effect of enteral supplementation of specific neutral and acidic oligosaccharides on the faecal microbiota and intestinal microenvironment in preterm infants. Eur J Clin Microbiol Infect Dis 32:269–276

    Article  CAS  Google Scholar 

  18. Shadid R, Haarman M, Knol J, Theis W, Beermann C, Rjosk-Dendorfer D, Schendel DJ, Koletzko BV, Krauss-Etschmann S (2007) Effects of galactooligosaccharide and long-chain fructooligosaccharide supplementation during pregnancy on maternal and neonatal microbiota and immunity—a randomized, double-blind, placebo-controlled study. Am J Clin Nutr 86:1426–1437

    CAS  Google Scholar 

  19. Magne F, Hachelaf W, Suau A, Boudraa G, Bouziane-Nedjadi K, Rigottier-Gois L, Touhami M, Desjeux JF, Pochart P (2008) Effects on faecal microbiota of dietary and acidic oligosaccharides in children during partial formula feeding. J Pediatr Gastroenterol Nutr 46:580–588

    Article  CAS  Google Scholar 

  20. Westerbeek EA, van den Berg A, Lafeber HN, Fetter WP, van Elburg RM (2011) The effect of enteral supplementation of a prebiotic mixture of non-human milk galacto-, fructo- and acidic oligosaccharides on intestinal permeability in preterm infants. Br J Nutr 105:268–274

    Article  CAS  Google Scholar 

  21. Osborn DA, Sinn JK (2013) Prebiotics in infants for prevention of allergy. Cochrane Database Syst Rev 3:CD006474. doi:10.1002/14651858.CD006474.pub3

    Google Scholar 

  22. Vos AP, Haarman M, Buco A, Govers M, Knol J, Garssen J, Stahl B, Boehm G, M’Rabet L (2006) A specific prebiotic oligosaccharide mixture stimulates delayed-type hypersensitivity in a murine influenza vaccination model. Int Immunopharmacol 6:1277–1286

    Article  CAS  Google Scholar 

  23. Vos AP, Haarman M, van Ginkel JW, Knol J, Garssen J, Stahl B, Boehm G, M’Rabet L (2007) Dietary supplementation of neutral and acidic oligosaccharides enhances Th1-dependent vaccination responses in mice. Pediatr Allergy Immunol 18:304–312

    Article  Google Scholar 

  24. Scholz-Ahrens KE, Acil Y, Schrezenmeir J (2002) Effect of oligofructose or dietary calcium on repeated calcium and phosphorus balances, bone mineralization and trabecular structure in ovariectomized rats*. Br J Nutr 88:365–377

    Article  CAS  Google Scholar 

  25. Reeves PG, Nielsen FH, Fahey GC (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951

    CAS  Google Scholar 

  26. Sapp RE, Davidson SD (1991) Microwave digestion of multi-component foods for sodium analysis by atomic absorption spectrometry. J Food Sci 56:1412–1414

    Article  CAS  Google Scholar 

  27. Elmer P (1971) Analytical method for atomic absorption spectrophotometry. P.E. Corp, Norwalk

    Google Scholar 

  28. Farley JR, Hall SL, Ilacas D, Orcutt C, Miller BE, Hill CS, Baylink DJ (1994) Quantification of skeletal alkaline phosphatase in osteoporotic serum by wheat germ agglutinin precipitation, heat inactivation, and a two-site immunoradiometric assay. Clin Chem 40:1749–1756

    CAS  Google Scholar 

  29. Mastaglia SR, Pellegrini GG, Mandalunis PM, Gonzales Chaves MM, Friedman SM, Zeni SN (2006) Vitamin D insufficiency reduces the protective effect of bisphosphonate on ovariectomy-induced bone loss in rats. Bone 39:837–844

    Article  CAS  Google Scholar 

  30. Zeni S, Gomez-Acotto C, Di Gregorio S, Mautalen C (2000) Differences in bone turnover and skeletal response to thyroid hormone treatment between estrogen-depleted and repleted rats. Calcif Tissue Int 67:173–177

    Article  CAS  Google Scholar 

  31. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res 2:595–610

    Article  CAS  Google Scholar 

  32. Fanaro S, Boehm G, Garssen J, Knol J, Mosca F, Stahl B, Vigi V (2005) Galacto-oligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: a review. Acta Paediatr 94:22–26

    Article  Google Scholar 

  33. Knol J, Scholtens P, Kafka C, Steenbakkers J, Gro S, Helm K, Klarczyk M, Schöpfer H, Böckler HM, Wells J (2005) Colon microflora in infants fed formula with galacto- and fructo-oligosaccharides: more like breast-fed infants. J Pediatr Gastroenterol Nutr 40:36–42

    Article  CAS  Google Scholar 

  34. Moro G, Minoli I, Mosca M, Fanaro S, Jelinek J, Stahl B, Boehm G (2002) Dosage-related bifidogenic effects of galacto- and fructooligosaccharides in formula-fed term infants. J Pediatr Gastroenterol Nutr 34:291–295

    Article  CAS  Google Scholar 

  35. Pérez-Conesa D, López G, Ros G (2007) Effects of probiotic, prebiotic and synbiotic follow-up infant formulas on large intestine morphology and bone mineralisation in rats. J Sci Food Agric 87:1059–1068

    Article  Google Scholar 

  36. Cummings JH, Macfarlane GT (1997) Role of intestinal bacteria in nutrient metabolism. JPEN 21:357–365

    Article  CAS  Google Scholar 

  37. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, Wolvers D, Watzl B, Szajewska H, Stahl B, Guarner F, Respondek F, Whelan K, Coxam V, Davicco MJ, Leotoing L, Wittrant Y, Delzenne NM, Cani PD, Neyrinck AM, Meheust A (2010) Prebiotic effects: metabolic and health benefits. Br J Nutr 104:S1–S63

    Article  CAS  Google Scholar 

  38. Bronner F, Pansu D (1999) Nutritional aspects of calcium absorption. J Nutr 129:9–12

    CAS  Google Scholar 

  39. Bronner F (2003) Mechanisms of intestinal calcium absorption. J Cell Biochem 88:387–393

    Article  CAS  Google Scholar 

  40. Scholz-Ahrens KE, Schrezenmeir J (2007) Inulin and oligofructose and mineral metabolism: the evidence from animal trials. J Nutr 137:2513S–2523S

    CAS  Google Scholar 

  41. Coudray C, Rambeau M, Feillet-Coudray C, Gueux E, Tressol JC, Mazur A, Rayssiguier Y (2005) Study of magnesium bioavailability from ten organic and inorganic Mg salts in Mg-depleted rats using a stable isotope approach. Magnes Res 18:215–223

    CAS  Google Scholar 

  42. Hardwick LL, Jones MR, Brautbar N, Lee DB (1991) Magnesium absorption: mechanisms and the influence of vitamin D, calcium and phosphate. J Nutr 121:13–23

    CAS  Google Scholar 

  43. Coudray C, Tressol JC, Gueux E, Rayssiguier Y (2003) Effects of inulin-type fructans of different chain length and type of branching on intestinal absorption and balance of calcium and magnesium in rats. Eur J Nutr 42:91–98

    Article  CAS  Google Scholar 

  44. Alfrey AC, Miller NL (1973) Bone magnesium pools in uremia. J Clin Invest 52:3019–3027

    Article  CAS  Google Scholar 

  45. Jahnen-Dechent W, Ketteler M (2012) Magnesium basics. Clin Kidney J 5:i3–i14

    Article  CAS  Google Scholar 

  46. Burr DB, Robling AG, Turner CH (2002) Effects of biomechanical stress on bones in animals. Bone 30:781–786

    Article  Google Scholar 

  47. Yuan G, Lu H, Yin Z, Dai S, Jia R, Xu J, Song X, Li L (2014) Effects of mixed subchronic lead acetate and cadmium chloride on bone metabolism in rats. Int J Clin Exp Med 7:1378–1385

    Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge Nutricia-Bago for kindly providing the GOS/FOS® mixture. The authors thank Ms. Julia Somoza for her technical assistance and Mr. Ricardo Orzuza from the General and Oral Biochemistry Department, School of Dentistry, Buenos Aires University, for his technical support and for taking care of the animals. This study was partially funded by the Buenos Aires University and CONICET Grant PIP 11220100100004.

Conflict of interest

The authors declare that there is no conflict of interest associated with this manuscript.

Author information

Authors and Affiliations

  1. General and Oral Biochemistry Department, School of Dentistry, Buenos Aires University (UBA), Buenos Aires, Argentina

    Gabriel Bryk, Gretel Pellegrini & Susana Noemí Zeni

  2. Metabolic Bone Diseases Laboratory, Clinical Hospital, Immunology, Genetic and Metabolism Institute (INIGEM), National Council for Scientific and Technologic Research (CONICET), Buenos Aires University (UBA), Av. Córdoba 2351-8vo. Piso, 1120, Buenos Aires, Argentina

    Gabriel Bryk, Magalí Zeni Coronel, Gretel Pellegrini & Susana Noemí Zeni

  3. Histology and Embryology Department, School of Dentistry, Buenos Aires University (UBA), Buenos Aires, Argentina

    Patricia Mandalunis

  4. National Council for Scientific and Technologic Research (CONICET), Buenos Aires, Argentina

    María Ester Rio

  5. Food Science and Nutritional Department, School of Pharmacy and Biochemistry, Buenos Aires University (UBA), Buenos Aires, Argentina

    María Luz Pita Martín de Portela

Authors
  1. Gabriel Bryk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Magalí Zeni Coronel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gretel Pellegrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patricia Mandalunis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. María Ester Rio
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. María Luz Pita Martín de Portela
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Susana Noemí Zeni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susana Noemí Zeni.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bryk, G., Coronel, M.Z., Pellegrini, G. et al. Effect of a combination GOS/FOS® prebiotic mixture and interaction with calcium intake on mineral absorption and bone parameters in growing rats. Eur J Nutr 54, 913–923 (2015). https://doi.org/10.1007/s00394-014-0768-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-014-0768-y

Keywords

Search

Navigation