The effect of fructan-enriched diet on bone turnover parameters in ovariectomized rats under calcium restriction
More details
Hide details
Department of Nutrition Technology and Consumption, Faculty of Food Technology, University of Agriculture, Krakow, Poland
Department of Animal Physiology, Faculty of Veterinary Medicine, University of Life Sciences, Lublin, Poland
Kinga Topolska   

University of Agriculture in Krakow, Faculty of Food Technology, Balicka 122, 30-149, Kraków, Poland
Osteoporosis, the “quiet epidemic”, is one of the most serious threats to public health. It is known that estrogen plays a significant role in the regulation of bone turnover, and its loss at menopause causes osteoporosis. Added to this, insufficient calcium intake accelerates bone mass loss, increasing the risk of fractures.

The study aimed to answer the question whether a fructan-enriched diet could be helpful in preventing from disturbances in bone turnover caused by calcium restriction combined with ovariectomy-induced estrogen deficiency. The differences related to the kind of fructan and ‘matrix effect’ of fructan action (form of addition) were also evaluated.

Material and methods:
The study was conducted using sham-operated (control groups) or ovariectomized (OVX) rats fed a calcium restricted diet. The treatment diets contained one of three fructan sources – Jerusalem artichoke, yacon and Beneo Orafti Synergy1 – added alone or as an ingredient of strawberry sorbet, all in the amount providing 8% fructans. Analyses of biological material included: serum Ca, Mg and P concentrations, alkaline phosphatase activity (ALP), osteocalcin (OC) and C-telopeptide degradation products from type I collagen (CTX). Densitometric parameters of femora were also assayed.

Among markers of bone turnover, the ALP activity depended both on the kind of fructan and the form of addition. The highest value was shown in the OVX group fed a low-calcium diet, whereas administration of diet enriched with Jerusalem artichoke led to an almost 50% decrease in the value of this parameter. Dietary fructans also lowered the OC level. Feeding rats with diet containing sorbet enriched in yacon or Jerusalem artichoke resulted in a decrease of CTX, compared to the diet containing yacon alone or fructan formulation in both forms No significant differences were observed in densitometric parameters between treatment groups.

The study was founded by the National Science Centre Poland project, on the basis of Decision No. DEC-2011/01/B/ NZ9/03045.
Feng X, McDonald JM. Disorders of Bone Remodeling. Annu Rev Pathol. 2011; 6: 121–145.
El Khassawna T, Böcker W, Govindarajan P, Schliefke N, Hürter B, Kampschulte M., Schlewitz G, Alt V, Lips KS, Faulenbach M., Möllmann H, Zahner D, Dürselen L, Ignatius A, Bauer N, Wenisch S, Langheinrich AC, Schnettler R, Heiss C. Effects of multi-deficiencies-diet on bone parameters of peripheral bone in ovariectomized mature rat. PloS ONE. 2013; 8(8): e71665.
World Health Organization. Assessment of Osteoporosis at the Primary Health Care Level. Report of a WHO Scientific Group. Geneva: WHO 2007.
Bonjour JP, Kohrt W, Levasseur R, Warren M, Whiting S, Kraenzlin M. Biochemical markers for assessment of calcium economy and bone metabolism: application in clinical trials from pharmaceutical agents to nutritional products. Nutr Res Rev. 2014; 27(2): 252–67.
Tu M-Y, Chen H-L, Tung Y-T, Kao C-C, Hu F-C, Chen C-M Short-Term Effects of Kefir-Fermented Milk Consumption on Bone Mineral Density and Bone Metabolism in a Randomized Clinical Trial of Osteoporotic Patients. PLoS ONE. 2015; 10(12): e0144231. doi:10.1371/journal.pone.014423.
Wang Q, Zi C-T, Wang J, Wang Y-N, Huang Y-W, Fu X-Q, Wang X-J and Sheng J. Dendrobium officinale Orchid Extract Prevents Ovariectomy-Induced Osteoporosis in Vivo and Inhibits RANKL-Induced Osteoclast Differentiation in Vitro. Front Pharmacol. 2018; 8: 966.
Liu T, Ding S, Yin D, Cuan X, Xie C, Xu H, Wang X, Sheng J. Pu-erh tea extract ameliorates ovariectomy-induced osteoporosis in rats and suppresses osteoclastogenesis in vitro. Front Pharmacol. 2017; 8: 324.
Price CT, Langford JR, Liporace FA. Essential Nutrients for Bone Health and a Review of their Availability in the Average North American Diet. The Open Orthopaed J. 2012; 6: 143–149.
Curtis EM, Moon RJ, Dennison EM, Harvey NC, Cooper C. Recent advances in the pathogenesis and treatment of osteoporosis. Clin Med. 2016; 16: 360–364.
Whisner CM, Castillo LF. Prebiotics, Bone and Mineral Metabolism Calcif Tissue Int. 2018; 102: 443.
Sabater-Molina M, Larque´ E, Torrella F, Zamora S. Dietary fructooligosaccharides and potential benefits on health. J Physiol Biochem. 2009; 65: 315–328.
Kolida S, Gibson GR. Prebiotic Capacity of Inulin-Type Fructans J Nutr. 2007; 137,11:1. Pages 2503S–2506S.
Franco-Robles E, López MG. Implication of Fructans in Health: Immunomodulatory and Antioxidant Mechanisms. Sci World J. 2015; Article ID 289267, 15 pages,
Roberfroid MB. Inulin-type fructans: functional food ingredients. J Nutr. 2007; 137: 2493S–2502S.
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, Léotoing L, Wittrant Y, Delzenne NM, Cani PD, Neyrinck AM, Meheust A.Prebiotic effects: metabolic and health benefits. Br J Nutr. 2010; 104(Suppl): S1–S63.
Topolska K, Filipiak-Florkiewicz A, Florkiewicz A, Cieślik E. Fructan stability in strawberry sorbets in dependence on their source and the period of storage. Eur Food Res Technol. 2017; 243: 701–709.
Cieślik E, Topolska K, Pisulewski PM. Effect of inulin-type fructans on body weight gain and selected biochemical parameters at calcium hypoalimentation in rats. Pol J Food Nutr Sci. 2009; 59(2): 163–168.
Cieślik E, Florkiewicz A, Filipiak-Florkiewicz A. [Quality of fruit juices with fructans additions]. Żyw Człow Metab. 2003; 3: 1027–1030. Polish.
Praznik W, Cieślik E, Filipiak-Florkiewicz A. Soluble dietary fibres in Jerusalem artichoke powders: composition and application in bread. Nahrung 2002; 46(3): 151–157.
Żary-Sikorska E, Juśkiewicz J. Effect of fructans with different degrees of polymerization on bacterial enzymes activity, lipid profile and antioxidant status in rats. Pol J Food Nutr Sci. 2008; 58(2): 269–272.
Domazetovic V, Marcucci G, Iantomasi T, Brandi ML, Vincenzini MT. Oxidative stress in bone remodeling: role of antioxidants Clin Cases Miner Bone Metab. 2017; 14(2): 209–216.
Johnston BD, Ward WE. The Ovariectomized Rat as a Model for Studying Alveolar Bone Loss in Postmenopausal Women. BioMed Res Int. 2015; Article ID 635023, 12 pages,
French DL, Muir JM, Webber CE. The ovariectomized, mature rat model of postmenopausal osteoporosis: an assessment of the bone sparing effects of curcumin. Phytomed. 2008; 15: 1069–1078.
Yamauchi H, Kushida K, Yamazaki K, Inoue T. Assessment of spine bone mineral density in ovariectomized rats using DXA. J Bone Miner Res. 1995; 10: 1033–1039.
Reeves PG, Nielsen FH, Fahey GC Jr. 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. 1993; 123(11): 1939–1951.
Karpouzos A, Diamantis E, Farmaki P, Savvanis S, Troupis T. Nutritional Aspects of Bone Health and Fracture Healing, J Osteoporos. 2017; Article ID 4218472, 10 pages,
Ye Q, Ma XQ, Hu CL, Lin B, Xu LS, Zheng CJ, Qin LP. Antiosteoporotic activity and constituents of Podocarpium podocarpum. Phytomed. 2015; 22: 94–102. doi:10.1016/j.phymed.2014.11.004.
Topolska K, Radzki RP, Filipiak-Florkiewicz A. Florkiewicz A., Leszczyńska T., Cieślik E. Fructan-Enriched Diet Increases Bone Quality in Female Growing Rats at Calcium Deficiency. Plant Foods Hum Nutr. 2018; 73(3): 172–179.
Raschka L, Daniel H. Mechanisms underlying the effects of inulin-type fructans on calcium absorption in the large intestine of rats. Bone. 2005; 37: 728–735.
Bryk G, Coronel MZ, Pellegrini G, Mandalunis P, Rio ME, de Portela ML, Zeni SN. 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 2015; 54: 913–923.
Kim YY, Jang KH, Lee EY. Cho Y, Kang SA, Ha WK, Choue R. The effect of chicory fructan fiber on calcium absorption and bone metabolism in Korean postmenopausal women. Nutr Sci. 2004; 7(3): 151–157.
Scholz-Ahrens KE, Schrezenmeir J. Inulin and oligofructose and mineral metabolism: the evidence from animal trials. J Nutr. 2007; 137(11 Suppl): 2513S–2523S.
Muthusami S, Ramachandran I, Muthusamy B, Vasudevan G, Prabhu V, Subramaniam V, Jagadeesan A, Narasimhan S. Ovariectomy induces oxidative stress and impairs bone antioxidant system in adult rats. Clin Chim Acta. 2005; 360: 81–86.
Baek KH, Oh KW, Lee WY, Lee SS, Kim MK, Kwon HS, Rhee EJ, Han JH, Song KH, Cha BY, Lee KW, Kang MI. Association of oxidative stress with postmenopausal osteoporosis and the effects of hydrogen peroxide on osteoclast formation in human bone marrow cell cultures. Calcif Tissue Int. 2010; 87: 226–235.
Pasqualetti V, Altomar, A, Guarino MPL, Locato V, Cocca S, Cimini S, Palma R, Alloni RAND De Gara L, Cicala M. Antioxidant Activity of Inulin and Its Role in the Prevention of Human Colonic Muscle Cell Impairment Induced by Lipopolysaccharide Mucosal Exposure, PLOS ONE. 2014; 9(5): e98031.
Giampieri F, Tulipani S, Alvarez-Suarez JM, Quiles JL, Mezzetti B, Battino M. The strawberry: composition, nutritional quality, and impact on human health. Nutrition. 2012; 28(1): 9–19 doi: 10.1016/j.nut.2011.08.009.
Ostman B, Michaelsson K, Helmersson J, Byberg L, Gedeborg R, Melhus H, Basu S. Oxidative stress and bone mineral density in elderly men: antioxidant activity of alpha-tocopherol. Free Radic Biol Med. 2009; 47: 668–673.
Kuo TR, Chen CH. Bone biomarker for the clinical assessment of osteoporosis: recent developments and future perspectives. Biomarker Res. 2017, 5: 18.
Liu T, Ding S, Yin D, Cuan X, Xie C, Xu H, Wang X, Sheng J. Pu-erh tea extract ameliorates ovariectomy-induced osteoporosis in rats and suppresses osteoclastogenesis in vitro. Front Pharmacol. 2018, 8: 324.
Lobo AR, Colli C, Filisetti T. Fructooligosaccharides improve bone mass and biomechanical properties in rats. Nutr Res. 2006; 26: 413–420.
Legette LL, Lee W, Martin BR, Story JA, Cambell JA, Weaver CM. Prebiotics enhance magnesium absorption and inulin-based fibers exert chronic effects on calcium utilization in a postmenopausal rodent model. J Food Sci. 2012; 77: H88–H94.
Demigné C, Jacobs H, Moundras C, Davicco MJ, Horcajada MN, Bernalier A, Coxam V. Comparison of native or reformulated chicory fructans, or non-purified chicory, on rat cecal fermentation and mineral metabolism. Eur J Nutr. 2008; 47(7): 366–374.