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Erschienen in: European Journal of Nutrition 7/2019

24.09.2018 | Original Contribution

Effects of probiotics, prebiotics or synbiotics on jawbone in obese-insulin resistant rats

verfasst von: Sathima Eaimworawuthikul, Wannipa Tunapong, Titikorn Chunchai, Sakawdaurn Yasom, Keerati Wanchai, Panan Suntornsaratoon, Narattaphol Charoenphandhu, Parameth Thiennimitr, Nipon Chattipakorn, Siriporn C. Chattipakorn

Erschienen in: European Journal of Nutrition | Ausgabe 7/2019

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Abstract

Purpose

Chronic high-fat diet (HFD) consumption results in gut dysbiosis, systemic inflammation, obese-insulin resistance, and osteoporosis of the jawbones. The probiotics, prebiotics or synbiotics alleviated gut dysbiosis and the metabolic disturbance in HFD-induced obesity. However, the effects on jawbone properties have not been investigated. This study aimed to investigate the effects of probiotic Lactobacillus paracasei HII01, prebiotic xylooligosaccharide (XOS), and synbiotics on the jawbone properties along with metabolic parameters, gut and systemic inflammation in HFD-fed rats.

Methods

Forty-eight male Wistar rats were fed with either a HFD or normal diet for 12 weeks. Rats in each group were subdivided into four subgroups to be treated with either vehicle, probiotics, prebiotics, or synbiotics for the additional 12 weeks. Blood samples, gut, bone marrows, and jawbones were collected to determine metabolic parameters, inflammation, and bone properties.

Results

The HFD-fed rats developed obese-insulin resistance, as indicated by increased body weight, dyslipidemia and decreased insulin sensitivity. Serum lipopolysaccharide levels and interleukin-6 mRNA expression in the ileum and bone marrows were elevated. Altered bone metabolism and the impaired jawbone properties were evident as indicated by decreased bone mineral density with increased trabecular separation. Reduced ultimate load and stiffness were observed in HFD-fed rats. Treatments with probiotics, prebiotics or synbiotics in HFD-fed rats improved metabolic parameters and reduced inflammation. However, no alterations in jawbone properties were found in all treatments.

Conclusion

The osteoporosis of the jawbone occurred in obese-insulin resistance, and treatments with probiotics, prebiotics and synbiotics were not sufficient to improve the jawbone properties.
Literatur
1.
Zurück zum Zitat Correction NM, Wang H, Lozano R, Davis A, Liang X, Zhou M, Vollset SE, Ozgoren AA, Abdalla S, Abd-Allah F (2015) Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013. Lancet 385(9963):117–171CrossRef Correction NM, Wang H, Lozano R, Davis A, Liang X, Zhou M, Vollset SE, Ozgoren AA, Abdalla S, Abd-Allah F (2015) Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013. Lancet 385(9963):117–171CrossRef
2.
Zurück zum Zitat Potikanond S, Rattanachote P, Pintana H, Suntornsaratoon P, Charoenphandhu N, Chattipakorn N, Chattipakorn S (2016) Obesity does not aggravate osteoporosis or osteoblastic insulin resistance in orchiectomized rats. J Endocrinol 228(2):85–95PubMedCrossRef Potikanond S, Rattanachote P, Pintana H, Suntornsaratoon P, Charoenphandhu N, Chattipakorn N, Chattipakorn S (2016) Obesity does not aggravate osteoporosis or osteoblastic insulin resistance in orchiectomized rats. J Endocrinol 228(2):85–95PubMedCrossRef
3.
Zurück zum Zitat Pramojanee SN, Phimphilai M, Kumphune S, Chattipakorn N, Chattipakorn SC (2013) Decreased jaw bone density and osteoblastic insulin signaling in a model of obesity. J Dent Res 92(6):560–565PubMedCrossRef Pramojanee SN, Phimphilai M, Kumphune S, Chattipakorn N, Chattipakorn SC (2013) Decreased jaw bone density and osteoblastic insulin signaling in a model of obesity. J Dent Res 92(6):560–565PubMedCrossRef
4.
Zurück zum Zitat Khamaisi M, Regev E, Yarom N, Avni B, Leitersdorf E, Raz I, Elad S (2007) Possible association between diabetes and bisphosphonate-related jaw osteonecrosis. J Clin Endocrinol Metab 92:1172–1175PubMedCrossRef Khamaisi M, Regev E, Yarom N, Avni B, Leitersdorf E, Raz I, Elad S (2007) Possible association between diabetes and bisphosphonate-related jaw osteonecrosis. J Clin Endocrinol Metab 92:1172–1175PubMedCrossRef
5.
Zurück zum Zitat Wessel JH, Dodson TB, Zavras AI (2008) Zoledronate, smoking, and obesity are strong risk factors for osteonecrosis of the jaw: a case-control study. J Oral Maxillofac Surg 66:625–631PubMedPubMedCentralCrossRef Wessel JH, Dodson TB, Zavras AI (2008) Zoledronate, smoking, and obesity are strong risk factors for osteonecrosis of the jaw: a case-control study. J Oral Maxillofac Surg 66:625–631PubMedPubMedCentralCrossRef
6.
Zurück zum Zitat Eaimworawuthikul S, Thiennimitr P, Chattipakorn N, Chattipakorn SC (2017) Diet-induced obesity, gut microbiota and bone, including alveolar bone loss. Arch Oral Biol 78:65–81PubMedCrossRef Eaimworawuthikul S, Thiennimitr P, Chattipakorn N, Chattipakorn SC (2017) Diet-induced obesity, gut microbiota and bone, including alveolar bone loss. Arch Oral Biol 78:65–81PubMedCrossRef
7.
Zurück zum Zitat Blasco-Baque V, Serino M, Vergnes JN, Riant E, Loubieres P, Arnal JF, Gourdy P, Sixou M, Burcelin R, Kemoun P (2012) High-fat diet induces periodontitis in mice through lipopolysaccharides (LPS) receptor signaling: protective action of estrogens. PLoS One 7(11):e48220PubMedPubMedCentralCrossRef Blasco-Baque V, Serino M, Vergnes JN, Riant E, Loubieres P, Arnal JF, Gourdy P, Sixou M, Burcelin R, Kemoun P (2012) High-fat diet induces periodontitis in mice through lipopolysaccharides (LPS) receptor signaling: protective action of estrogens. PLoS One 7(11):e48220PubMedPubMedCentralCrossRef
8.
Zurück zum Zitat Li Y, Lu Z, Zhang X, Yu H, Kirkwood KL, Lopes-Virella MF, Huang Y (2015) Metabolic syndrome exacerbates inflammation and bone loss in periodontitis. J Dent Res 94(2):362–370PubMedPubMedCentralCrossRef Li Y, Lu Z, Zhang X, Yu H, Kirkwood KL, Lopes-Virella MF, Huang Y (2015) Metabolic syndrome exacerbates inflammation and bone loss in periodontitis. J Dent Res 94(2):362–370PubMedPubMedCentralCrossRef
9.
Zurück zum Zitat Benites BD, Gilli SC, Saad ST (2014) Obesity and inflammation and the effect on the hematopoietic system. Rev Bras Hematol Hemoter 36(2):147–151PubMedPubMedCentralCrossRef Benites BD, Gilli SC, Saad ST (2014) Obesity and inflammation and the effect on the hematopoietic system. Rev Bras Hematol Hemoter 36(2):147–151PubMedPubMedCentralCrossRef
10.
Zurück zum Zitat Luo Y, Chen GL, Hannemann N, Ipseiz N, Kronke G, Bauerle T, Munos L, Wirtz S, Schett G, Bozec A (2015) Microbiota from obese mice regulate hematopoietic stem cell differentiation by altering the bone niche. Cell Metab 22(5):886–894PubMedCrossRef Luo Y, Chen GL, Hannemann N, Ipseiz N, Kronke G, Bauerle T, Munos L, Wirtz S, Schett G, Bozec A (2015) Microbiota from obese mice regulate hematopoietic stem cell differentiation by altering the bone niche. Cell Metab 22(5):886–894PubMedCrossRef
11.
Zurück zum Zitat da Silva SV, Renovato-Martins M, Ribeiro-Pereira C, Citelli M, Barja-Fidalgo C (2016) Obesity modifies bone marrow microenvironment and directs bone marrow mesenchymal cells to adipogenesis. Obesity (Silver Spring Md) 24(12):2522–2532CrossRef da Silva SV, Renovato-Martins M, Ribeiro-Pereira C, Citelli M, Barja-Fidalgo C (2016) Obesity modifies bone marrow microenvironment and directs bone marrow mesenchymal cells to adipogenesis. Obesity (Silver Spring Md) 24(12):2522–2532CrossRef
12.
Zurück zum Zitat Ejtahed HS, Soroush AR, Angoorani P, Larijani B, Hasani-Ranjbar S (2016) Gut microbiota as a target in the pathogenesis of metabolic disorders: a new approach to novel therapeutic agents. Horm Metab Res 48(06):349–358PubMedCrossRef Ejtahed HS, Soroush AR, Angoorani P, Larijani B, Hasani-Ranjbar S (2016) Gut microbiota as a target in the pathogenesis of metabolic disorders: a new approach to novel therapeutic agents. Horm Metab Res 48(06):349–358PubMedCrossRef
14.
Zurück zum Zitat Ojeda P, Bobe A, Dolan K, Leone V, Martinez K (2016) Nutritional modulation of gut microbiota—the impact on metabolic disease pathophysiology. J Nutr Biochem 28:191–200PubMedCrossRef Ojeda P, Bobe A, Dolan K, Leone V, Martinez K (2016) Nutritional modulation of gut microbiota—the impact on metabolic disease pathophysiology. J Nutr Biochem 28:191–200PubMedCrossRef
15.
Zurück zum Zitat de La Serre CB, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE (2010) Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol 299(2):G440–G448CrossRef de La Serre CB, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE (2010) Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol 299(2):G440–G448CrossRef
16.
Zurück zum Zitat Kim KA, Gu W, Lee IA, Joh EH, Kim DH (2012) High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One 7(10):e47713PubMedPubMedCentralCrossRef Kim KA, Gu W, Lee IA, Joh EH, Kim DH (2012) High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One 7(10):e47713PubMedPubMedCentralCrossRef
17.
Zurück zum Zitat Shin NR, Whon TW, Bae JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33(9):496–503PubMedCrossRef Shin NR, Whon TW, Bae JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33(9):496–503PubMedCrossRef
18.
Zurück zum Zitat Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56(7):1761–1772PubMedCrossRef Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56(7):1761–1772PubMedCrossRef
19.
Zurück zum Zitat Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, Backhed F, Ohlsson C (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27(6):1357–1367PubMedPubMedCentralCrossRef Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, Backhed F, Ohlsson C (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27(6):1357–1367PubMedPubMedCentralCrossRef
20.
Zurück zum Zitat Flint HJ, Scott KP, Louis P, Duncan SH (2012) The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9(10):577–589PubMedCrossRef Flint HJ, Scott KP, Louis P, Duncan SH (2012) The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9(10):577–589PubMedCrossRef
21.
Zurück zum Zitat Tunapong W, Apaijai N, Yasom S, Tanajak P, Wanchai K, Chunchai T, Kerdphoo S, Eaimworawuthikul S, Thiennimitr P, Pongchaidecha A, Lungkaphin A, Pratchayasakul W, Chattipakorn SC, Chattipakorn N (2017) Chronic treatment with prebiotics, probiotics and synbiotics attenuated cardiac dysfunction by improving cardiac mitochondrial dysfunction in male obese insulin-resistant rats. Eur J Nutr. https://doi.org/10.1007/s00394-017-1482-3 PubMedCrossRef Tunapong W, Apaijai N, Yasom S, Tanajak P, Wanchai K, Chunchai T, Kerdphoo S, Eaimworawuthikul S, Thiennimitr P, Pongchaidecha A, Lungkaphin A, Pratchayasakul W, Chattipakorn SC, Chattipakorn N (2017) Chronic treatment with prebiotics, probiotics and synbiotics attenuated cardiac dysfunction by improving cardiac mitochondrial dysfunction in male obese insulin-resistant rats. Eur J Nutr. https://​doi.​org/​10.​1007/​s00394-017-1482-3 PubMedCrossRef
22.
Zurück zum Zitat Chunchai T, Thunapong W, Yasom S, Wanchai K, Eaimworawuthikul S, Metzler G, Lungkaphin A, Pongchaidecha A, Sirilun S, Chaiyasut C, Pratchayasakul W, Thiennimitr P, Chattipakorn N, Chattipakorn SC (2018) Decreased microglial activation through gut-brain axis by prebiotics, probiotics, or synbiotics effectively restored cognitive function in obese-insulin resistant rats. J Neuroinflamm 15(1):11CrossRef Chunchai T, Thunapong W, Yasom S, Wanchai K, Eaimworawuthikul S, Metzler G, Lungkaphin A, Pongchaidecha A, Sirilun S, Chaiyasut C, Pratchayasakul W, Thiennimitr P, Chattipakorn N, Chattipakorn SC (2018) Decreased microglial activation through gut-brain axis by prebiotics, probiotics, or synbiotics effectively restored cognitive function in obese-insulin resistant rats. J Neuroinflamm 15(1):11CrossRef
23.
Zurück zum Zitat Suntornsaratoon P, Krishnamra N, Charoenphandhu N (2015) Positive long-term outcomes from presuckling calcium supplementation in lactating rats and the offspring. Am J Physiol Endocrinol Metab 308(11):E1010–E1022PubMedCrossRef Suntornsaratoon P, Krishnamra N, Charoenphandhu N (2015) Positive long-term outcomes from presuckling calcium supplementation in lactating rats and the offspring. Am J Physiol Endocrinol Metab 308(11):E1010–E1022PubMedCrossRef
24.
Zurück zum Zitat Haffner SM, Miettinen H, Stern MP (1997) The homeostasis model in the San Antonio heart study. Diabetes Care 20(7):1087–1092PubMedCrossRef Haffner SM, Miettinen H, Stern MP (1997) The homeostasis model in the San Antonio heart study. Diabetes Care 20(7):1087–1092PubMedCrossRef
25.
Zurück zum Zitat Peinnequin A, Mouret C, Birot O, Alonso A, Mathieu J, Clarencon D, Agay D, Chancerelle Y, Multon E (2004) Rat pro-inflammatory cytokine and cytokine related mRNA quantification by real-time polymerase chain reaction using SYBR green. BMC Immunol 5(1):3PubMedPubMedCentralCrossRef Peinnequin A, Mouret C, Birot O, Alonso A, Mathieu J, Clarencon D, Agay D, Chancerelle Y, Multon E (2004) Rat pro-inflammatory cytokine and cytokine related mRNA quantification by real-time polymerase chain reaction using SYBR green. BMC Immunol 5(1):3PubMedPubMedCentralCrossRef
26.
Zurück zum Zitat Abbassy MA, Watari I, Soma K (2010) The effect of diabetes mellitus on rat mandibular bone formation and microarchitecture. Eur J Oral Sci 118(4):364–369PubMedCrossRef Abbassy MA, Watari I, Soma K (2010) The effect of diabetes mellitus on rat mandibular bone formation and microarchitecture. Eur J Oral Sci 118(4):364–369PubMedCrossRef
27.
Zurück zum Zitat Jiang GZ, Matsumoto H, Hori M, Gunji A, Hakozaki K, Akimoto Y, Fujii A (2008) Correlation among geometric, densitometric, and mechanical properties in mandible and femur of osteoporotic rats. J Bone Miner Metab 26(2):130–137PubMedCrossRef Jiang GZ, Matsumoto H, Hori M, Gunji A, Hakozaki K, Akimoto Y, Fujii A (2008) Correlation among geometric, densitometric, and mechanical properties in mandible and femur of osteoporotic rats. J Bone Miner Metab 26(2):130–137PubMedCrossRef
28.
Zurück zum Zitat Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8(6):e1000412PubMedPubMedCentralCrossRef Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8(6):e1000412PubMedPubMedCentralCrossRef
29.
Zurück zum Zitat Vasikaran S, Cooper C, Eastell R, Griesmacher A, Morris HA, Trenti T, Kanis JA (2011) International osteoporosis foundation and international federation of clinical chemistry and laboratory medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med 49(8):1271–1274PubMedCrossRef Vasikaran S, Cooper C, Eastell R, Griesmacher A, Morris HA, Trenti T, Kanis JA (2011) International osteoporosis foundation and international federation of clinical chemistry and laboratory medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med 49(8):1271–1274PubMedCrossRef
30.
Zurück zum Zitat Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature 487(7405):104–108PubMedPubMedCentralCrossRef Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature 487(7405):104–108PubMedPubMedCentralCrossRef
31.
Zurück zum Zitat Martinez-Medina M, Denizot J, Dreux N, Robin F, Billard E, Bonnet R, Darfeuille-Michaud A, Barnich N (2014) Western diet induces dysbiosis with increased E coli in CEABAC10 mice, alters host barrier function favouring AIEC colonisation. Gut 63(1):116–124PubMedCrossRef Martinez-Medina M, Denizot J, Dreux N, Robin F, Billard E, Bonnet R, Darfeuille-Michaud A, Barnich N (2014) Western diet induces dysbiosis with increased E coli in CEABAC10 mice, alters host barrier function favouring AIEC colonisation. Gut 63(1):116–124PubMedCrossRef
32.
Zurück zum Zitat Li Z, Summanen PH, Komoriya T, Finegold SM (2015) In vitro study of the prebiotic xylooligosaccharide (XOS) on the growth of Bifidobacterium spp. and Lactobacillus spp. Int J Food Sci Nutr 66(8):919–922PubMedCrossRef Li Z, Summanen PH, Komoriya T, Finegold SM (2015) In vitro study of the prebiotic xylooligosaccharide (XOS) on the growth of Bifidobacterium spp. and Lactobacillus spp. Int J Food Sci Nutr 66(8):919–922PubMedCrossRef
33.
Zurück zum Zitat Nagpal R, Kaur A (2011) Synbiotic effect of various prebiotics on in vitro activities of probiotic lactobacilli. Ecol Food Nutr 50(1):63–68PubMedCrossRef Nagpal R, Kaur A (2011) Synbiotic effect of various prebiotics on in vitro activities of probiotic lactobacilli. Ecol Food Nutr 50(1):63–68PubMedCrossRef
34.
Zurück zum Zitat Scholz-Ahrens KE, Adolphi B, Rochat F, Barclay DV, de Vrese M, Açil Y, Schrezenmeir J (2016) Effects of probiotics, prebiotics, and synbiotics on mineral metabolism in ovariectomized rats—impact of bacterial mass, intestinal absorptive area and reduction of bone turn-over. NFS J 3:41–50CrossRef Scholz-Ahrens KE, Adolphi B, Rochat F, Barclay DV, de Vrese M, Açil Y, Schrezenmeir J (2016) Effects of probiotics, prebiotics, and synbiotics on mineral metabolism in ovariectomized rats—impact of bacterial mass, intestinal absorptive area and reduction of bone turn-over. NFS J 3:41–50CrossRef
35.
Zurück zum Zitat Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Järvenpää S, Kautiainen H, Julkunen I, Vapaatalo H, Korpela R (2008) Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol 14(13):2029–2036PubMedPubMedCentralCrossRef Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Järvenpää S, Kautiainen H, Julkunen I, Vapaatalo H, Korpela R (2008) Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol 14(13):2029–2036PubMedPubMedCentralCrossRef
36.
Zurück zum Zitat Maekawa T, Hajishengallis G (2014) Topical treatment with probiotic Lactobacillus brevis CD2 inhibits experimental periodontal inflammation and bone loss. J Periodontal Res 49(6):785–791PubMedPubMedCentralCrossRef Maekawa T, Hajishengallis G (2014) Topical treatment with probiotic Lactobacillus brevis CD2 inhibits experimental periodontal inflammation and bone loss. J Periodontal Res 49(6):785–791PubMedPubMedCentralCrossRef
37.
Zurück zum Zitat Ohlsson C, Engdahl C, Fak F, Andersson A, Windahl SH, Farman HH, Moverare-Skrtic S, Islander U, Sjogren K (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One 9(3):e92368PubMedPubMedCentralCrossRef Ohlsson C, Engdahl C, Fak F, Andersson A, Windahl SH, Farman HH, Moverare-Skrtic S, Islander U, Sjogren K (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One 9(3):e92368PubMedPubMedCentralCrossRef
38.
Zurück zum Zitat Peerajan S, Chaiyasut C, Sirilun S, Chaiyasut K, Kesika P, Sivamaruthi BS (2016) Enrichment of nutritional value of Phyllanthus emblica fruit juice using the probiotic bacterium, Lactobacillus paracasei HII01 mediated fermentation. Food Sci Technol (Campinas) 36:116–123CrossRef Peerajan S, Chaiyasut C, Sirilun S, Chaiyasut K, Kesika P, Sivamaruthi BS (2016) Enrichment of nutritional value of Phyllanthus emblica fruit juice using the probiotic bacterium, Lactobacillus paracasei HII01 mediated fermentation. Food Sci Technol (Campinas) 36:116–123CrossRef
40.
Zurück zum Zitat Gatej SM, Marino V, Bright R, Fitzsimmons TR, Gully N, Zilm P, Gibson RJ, Edwards S, Bartold PM (2018) Probiotic Lactobacillus rhamnosus GG prevents alveolar bone loss in a mouse model of experimental periodontitis. J Clin Periodontol 45(2):204–212PubMedCrossRef Gatej SM, Marino V, Bright R, Fitzsimmons TR, Gully N, Zilm P, Gibson RJ, Edwards S, Bartold PM (2018) Probiotic Lactobacillus rhamnosus GG prevents alveolar bone loss in a mouse model of experimental periodontitis. J Clin Periodontol 45(2):204–212PubMedCrossRef
41.
Zurück zum Zitat Ricoldi MST, Furlaneto FAC, Oliveira LFF, Teixeira GC, Pischiotini JP, Moreira ALG, Ervolino E, de Oliveira MN, Bogsan CSB, Salvador SL, Messora MR (2017) Effects of the probiotic Bifidobacterium animalis subsp. lactis on the non-surgical treatment of periodontitis. A histomorphometric, microtomographic and immunohistochemical study in rats. PLoS One 12(6):e0179946PubMedPubMedCentralCrossRef Ricoldi MST, Furlaneto FAC, Oliveira LFF, Teixeira GC, Pischiotini JP, Moreira ALG, Ervolino E, de Oliveira MN, Bogsan CSB, Salvador SL, Messora MR (2017) Effects of the probiotic Bifidobacterium animalis subsp. lactis on the non-surgical treatment of periodontitis. A histomorphometric, microtomographic and immunohistochemical study in rats. PLoS One 12(6):e0179946PubMedPubMedCentralCrossRef
Metadaten
Titel
Effects of probiotics, prebiotics or synbiotics on jawbone in obese-insulin resistant rats
verfasst von
Sathima Eaimworawuthikul
Wannipa Tunapong
Titikorn Chunchai
Sakawdaurn Yasom
Keerati Wanchai
Panan Suntornsaratoon
Narattaphol Charoenphandhu
Parameth Thiennimitr
Nipon Chattipakorn
Siriporn C. Chattipakorn
Publikationsdatum
24.09.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 7/2019
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-018-1829-4

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