생명과학회지 (Journal of Life Science)

  • 제27권12호
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  • Pages.1421-1429
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  • 2017
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  • 1225-9918(pISSN)
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  • 2287-3406(eISSN)
한국생명과학회 (Korean Society of Life Science)
권호 표지
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흰 쥐에서 복합 유산균과 다시마가 항비만 및 장내 미생물에 미치는 영향

Effects of Mixture Lactic Acid Bacteria and Sea Tangle on Anti-obesity and Gut Microflora in Rats

  • 유다윤 (경남과학기술대학교 동물소재공학과) ;
  • 김정아 (경남과학기술대학교 동물소재공학과) ;
  • 김인성 (경남과학기술대학교 동물소재공학과) ;
  • 이철영 (경남과학기술대학교 동물소재공학과) ;
  • 김성찬 (한림대학교 의과대학) ;
  • 이상석 (순천대학교 동물자원과학과) ;
  • 최인순 (신라대학교 생명과학과) ;
  • 조광근 (경남과학기술대학교 동물소재공학과)
  • Yu, Da Yoon (Department of Animal Resources Technology, Gyeongnam National University of Science and Technology) ;
  • Kim, Jeong A (Department of Animal Resources Technology, Gyeongnam National University of Science and Technology) ;
  • Kim, In Sung (Department of Animal Resources Technology, Gyeongnam National University of Science and Technology) ;
  • Lee, Chul Young (Department of Animal Resources Technology, Gyeongnam National University of Science and Technology) ;
  • Kim, Seong chan (Colleges of Medicine, Hallym University) ;
  • Lee, Sang Suk (Department of Animal Science and Technology, Sunchon National University) ;
  • Choi, In Soon (Department of Life Science, Silla University) ;
  • Cho, Kwang Keun (Department of Animal Resources Technology, Gyeongnam National University of Science and Technology)
  • 투고 : 2017.11.14
  • 심사 : 2017.12.19
  • 발행 : 2017.12.30
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초록

본 연구에서는 유산균과 다시마가 항비만과 장내 미생물에 미치는 영향을 조사하기 위하여 8주령의 수컷 흰쥐를 1 cage 당 3 마리씩 4반복하여 처리군 당 12마리를 사용하였으며, 대조구 기초사료에 고지방사료 처리구는 10% lard를 첨가하고, 여기에 5% 유산균($5{\times}10^8cfu$, Lactobacillus rhamnosus, Lactobacillus johnsonii, Bifidobacterium longum, Bifidobacterium lactis) 첨가구, 5% 유산균과 10% 다시마를 혼합 첨가한 처리구로 구분하였다. 고지방사료 처리군에 비해 유산균 처리군과 다시마와 유산균 혼합 처리군은 체중과 일당 증체량의 감소를 나타내었다. 장내미생물을 pyrosequncing 방법으로 확인한 결과, 고지방사료 처리군에 비해 유산균 처리군과 다시마와 유산균 혼합 처리군은 Firmicutes 비율이 감소하고, Bacteroidetes의 비율이 증가하였으며, Firmicutes/Bacteroidetes (F/B) 비율은 감소하였다. 또한 이 두 처리군은 Firmicutes 문에 속하는 비만 관련 미생물 Roseburia, Mollicute, Erysipelotrichi, Oscillibacter가 감소하였고, 반면에 Bacteroidetes 문에 속하는 항비만 관련 미생물 Prevotella, Alistipes, Bacteroides는 증가하였다. 분변 내 단쇄지방산(short chain fatty acid; SCFA) 은 다시마와 유산균을 섭취한 처리군에서 butyric acid 함량이 높게 나타났다. 결론적으로, 다시마와 유산균의 혼합 처리는 항비만 효과를 나타내며 장내 미생물 변화를 유도하고 장내 대사 물질인 butyric acid의 함량을 높이는 것을 시사한다.

The present study was undertaken to investigate the effects of dietary provision of lactic acid bacteria (LB) and sea tangle (ST) on the obesity-associated intestinal microbiota in rats with obesity induced by a high-fat diet. Forty-eight 8-wk-old Sprague-Dawley rats were fed a basal diet (CON), a high fat diet (HFD; CON supplemented with 10% lard), HF supplemented with LB [HFL; $5{\times}10^8cfu$ of each of Lactobacillus rhamnosus, Lactobacillus johnsonii, Bifidobacterium longum and Bifidobacterium lactis], or HFL containing 10% ST (HFLS), with 4 replicates (cages) of 3 rats per dietary treatment, for 6 wk, and the intestinal microbiota were determined by pyrosequencing. The HFL and HFLS groups exhibited reduced rates of weight gain than the HF group, and the former groups had smaller ratios of Firmicutes and greater ratios of Bacteriodetes, with decreased Firmicutes/Bacteroidetes ratios, than the latter at the level of the phylum. Compared with the results for the HF group, HFL and HFLS had reduced ratios of the families of Roseburia, Mollicute, Erysipelotrichi, and Oscillibacter within Firmicutes associated with obesity and increased ratios of the families of Prevotella, Alistipes and Bacteroides within the Bacterioidetes phylum known to have an anti-obesity effect. The content of butyric acid in feces was greater in the HFLS group vs. HF and HFL. In conclusion, the present results suggest that dietary provision of LB plus ST has an anti-obesity effect and induced changes in intestinal microorganisms, and enhanced the content of butyric acid, which is an intestinal metabolite.

키워드

참고문헌

  1. Albu, J., Allison, D., Boozer, C. N., Heymsfield, S., Kissileff, H., Kretser, A., Krumhar, K., Leibel, R., Nonas, C., PiSunyer, X., VanItallie, T. and Wedral, E. 1997. Obesity solutions: report of a meeting. Nutr. Rev. 55, 150-156.
  2. Bagarolli, R. A., Tobar, N., Oliveira, A. G., Araujo, T. G., Carvalho, B. M., Rocha, G. Z., Vecina, J. F., Calisto, K., Guadagnini, D., Prada, P. O., Santos, A., Saad, S. T. O. and Saad, M. J. A. 2017. Probiotics modulate gut microbiota and improve insulin sensitivity in DIO mice. J. Nutr. Biochem. 50, 16-25. https://doi.org/10.1016/j.jnutbio.2017.08.006
  3. Barcenilla, A., Pryde, S. E., Martin, J. C., Duncan, S. H., Stewart, C. S., Henderson, C. and Flint, H. J. 2000. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl. Environ. Microbiol. 66, 1654-1661. https://doi.org/10.1128/AEM.66.4.1654-1661.2000
  4. Biagi, E., Candela, M., Fairweather-Tait, S., Franceschi, C. and Brigidi, P. 2012. Aging of the human metaorganism: the microbial counterpart. Age. (Dordr) 34, 247-267. https://doi.org/10.1007/s11357-011-9217-5
  5. Bobek, P., Ozdiin, L. and Galbavyy, S. 1998. Dose- and timedependent hypocholesterolemic effect of oyster mushroom (Pleurotus ostreatus) in rat. Nutrition 14, 282-286. https://doi.org/10.1016/S0899-9007(97)00471-1
  6. Branchereau, M., Reichardt, F., Loubieres, P., Marck, P., Waget, A., Azalbert, V., Colom, A., Padmanabhan, R., Iacovoni, J. S., Giry, A., Terce, F., Heymes, C., Burcelin, R., Serino, M. and Blasco-Baque, V. 2016. Periodontal dysbiosis linked to periodontitis is associated with cardiometabolic adaptation to high-fat diet in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 310, G1091-101. https://doi.org/10.1152/ajpgi.00424.2015
  7. Caldeira, D., Martins, C., Alves, L. B., Pereira, H., Ferreira, J. J. and Costa, J. 2013. Caffeine does not increase the risk of atrial fibrillation: a systematic review and meta-analysis of observational studies. Heart 99, 1383-1389. https://doi.org/10.1136/heartjnl-2013-303950
  8. Chen, J., Zhou, J., Wei, S., Xie, Z., Wen, C. and Xu, G. 2015. Effect of a traditional Chinese medicine prescription Quzhuotongbi decoction on hyperuricemia model rats studied by using serum metabolomics based on gas chromatography-mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 1026, 272-278.
  9. Cho, I. S., Han, Y. H., Lee, G. Y. and Park, K. Y. 2007. Search for medicinal plants on improvable effect of intestinal microflora. Kor. Soc. Med. Crop. Sci. 15, 26-29.
  10. Choi, H. J., Kil, J. H., Bak, S. S., Kong, C. S., Park, K. Y., Seo, Y. W. and Lim, S. Y. 2006. Inhibitory effects of solvent extracts from seven brown algae on mutagenicity and growth of human cancer cells. J. Life Sci. 16, 1080-1086. https://doi.org/10.5352/JLS.2006.16.7.1080
  11. Choi, J. S., Shin, S. H., Ha, Y. M., Kim, Y. C., Kim, T. B., Park, S. M., Choi, I. S., Song, H. J. and Choi, Y. J. 2008. Mineral contents and physiological activities of dried sea tangle (Laminaria japonica) collected from Gijang and Wando in Korea. J. Life Sci. 18, 474-481. https://doi.org/10.5352/JLS.2008.18.4.474
  12. Crescenzo, R., Mazzoli, A., Di Luccia, B., Bianco, F., Cancelliere, R., Cigliano, L., Liverini, G., Baccigalupi, L. and Iossa, S. 2017. Dietary fructose causes defective insulin signalling and ceramide accumulation in the liver that can be reversed by gut microbiota modulation. Food Nutr. Res. 61, 1331657. https://doi.org/10.1080/16546628.2017.1331657
  13. Cui, C. B., Lee, E. Y., Lee, D. S. and Ham, S. S. 2010. Antimutagenic and anticancer effects of ethanol extract from Korean traditional Doenjang added sea tangle. Kor. J. Food Sci. Technol. 42, 620-626.
  14. Duncan, D. B. 1955. Multiple range and multiple F tests. Biometrics 11, 1-42. https://doi.org/10.2307/3001478
  15. Duncan, S. H., Louis, P. and Flint, H. J. 2004. Lactate-utilizing bacteria, isolated from human feces that produce butyrate as a major fermentation product. Appl. Environ. Microbiol. 70, 5810-5817. https://doi.org/10.1128/AEM.70.10.5810-5817.2004
  16. Elinav, E., Strowig, T., Kau, A. L., Henao-Mejia, J., Thaiss, C. A., Booth, C. J., Peaper, D. R., Bertin, J., Eisenbarth, S. C., Gordon, J. I. and Flavell, R. A. 2011. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145, 745-757. https://doi.org/10.1016/j.cell.2011.04.022
  17. Falony, G., Verschaeren, A., De Bruycker, F., De Preter, V., Verbeke, K., Leroy, F. and De Vuyst, L. 2009. In vitro kinetics of prebiotic inulin-type fructan fermentation by butyrate-producing colon bacteria: implementation of online gas chromatography for quantitative analysis of carbon dioxide and hydrogen gas production. Appl. Environ. Microbiol. 75, 5884-5892. https://doi.org/10.1128/AEM.00876-09
  18. Filippo, C. D., Cavalieri, D., Paola, M. D., Ramazzotti, M., Poullet, J. B., Massart, S., Collini, S., Pieraccini, G. and Lionetti, P. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 33, 14691-1496.
  19. Grundy, S. M. 1988. Multifactorial causation of obesity: implications for prevention. J. Clin. Nutr. 67, 563S-72S.
  20. Hadwiger, L. A., Fristensky, B. and Riggleman, R. C. 1984. Chitosan, a natural regulator in plant-fungal pathogen interactions, increases crop yield. In: "Chitin, chitosan and related enzymes" (ed. Zikakis, J.P.) Academic Press Inc. Orlando, pp 291-298.
  21. Hakkak, R., Korourian, S., Foley, S. L. and Erickson, B. D. 2017. Assessment of gut microbiota populations in lean and obese Zucker rats. PLoS One 12, e0181451. https://doi.org/10.1371/journal.pone.0181451
  22. Hedemann, M. S., Theil, P. K. and Bach Knudsen, K. E. 2009. The thickness of the intestinal mucous layer in the colon of rats fed various sources of non-digestible carbohydrates is positively correlated with the pool of SCFA but negatively correlated with the proportion of butyric acid in digesta. Br. J. Nutr. 102, 117-25. https://doi.org/10.1017/S0007114508143549
  23. Henning, S. M., Yang, J., Shao, P., Lee, R. P., Huang, J., Ly, A., Hsu, M., Lu, Q. Y., Thames, G., Heber, D. and Li, Z. 2017. Health benefit of vegetable/fruit juice-based diet: Role of microbiome. Sci. Rep. 7, 2167. https://doi.org/10.1038/s41598-017-02200-6
  24. Horie, M., Miura, T., Hirakata, S., Hosoyama, A., Sugino, S., Umeno, A., Murotomi, K., Yoshida, Y. and Koike, T. 2017. Comparative analysis of the intestinal flora in type 2 diabetes and nondiabetic mice. Exp. Anim. 10, 1538.
  25. Hur, K. Y. and Lee, M. S. 2015. Gut microbiota and metabolic disorders. Diabetes Metab. J. 39, 198-203. https://doi.org/10.4093/dmj.2015.39.3.198
  26. Hwang, Y. J., Chae, I. S. and Lee, Y. K. 2017. Anti-inflammatory effects of fermented Laminaria japonica and Hizikia fusiforme water extracts with probiotics in LPS-stimulated RAW264.7 macrophage cell line. J. East Asian. Soc. Diet Life 27, 1-8. https://doi.org/10.17495/easdl.2017.2.27.1.1
  27. Ishiguro, T. 1984. Gas chromatographic studies on propionic acid, butyric acid and valeric acid in culture fluid of Trichomonas vaginalis. Nihon Sanka Fujinka Gakkai Zasshi 36, 363-8.
  28. Isolauri, E., Salminen, S. and Ouwehand, A. C. 2004. Microbial-gut interactions in health and disease, Probiotics. Best Pract. Res. Clin. Gastroenterol. 18, 299-313. https://doi.org/10.1016/j.bpg.2003.10.006
  29. Jang, W. S. and Choung, S. Y. 2013. Antiobesity effects of the ethanol extract of Laminaria japonica Areshoung in high-fat-diet-induced obese rat. Evid. Based. Complement. Alternat. Med. 2013, 17.
  30. Jun, H. S., Choi, Y. K., Won, Y. S., Hun, B. H. and Kim, J. W. 1999. Effects of lactic acid bacteria on infection of Salmonella typhimurium in mouse. J. Kor. Dairy Sci. 21, 171-182.
  31. Kang, C., Wang, B., Kaliannan, K., Wang, X., Lang, H., Hui, S., Huang, L., Zhang, Y., Zhou, M., Chen, M. and Mi, M. 2017. Gut microbiota mediates the protective effects of dietary capsaicin against chronic low-grade inflammation and associated obesity induced by high-fat diet. mBio. 8, e00470-17.
  32. Karimi, G., Jamaluddin, R., Mohtarrudin, N., Ahmad, Z., Khazaai, H. and Parvaneh, M. 2017. Single-species versus dual-species probiotic supplementation as an emerging therapeutic strategy for obesity. Nutr. Metab. Cardiovasc. Dis. 10, 910-918.
  33. Kim, B. S., Song, M. Y. and Kim, H. 2014. The anti-obesity effect of Ephedra sinica through modulation of gut microbiota in obese Korean women. J. Ethnopharmacol. 152, 532-539. https://doi.org/10.1016/j.jep.2014.01.038
  34. Kim, J. Y., Choi, E. Y., Hong, Y. H., Song, Y. O., Han, J. S., Lee, S. S., Han, E. S., Kim, T. W., Choi, I. S. and Cho, K. K. 2016. Changes in Korean adult females' intestinal microbiota resulting from kimchi intake. JNFS 6, 2-9.
  35. Kim, O. S., Cho, Y. J., Lee, K., Yoon, S. H., Kim, M., Na, H., Park, S. C., Jeon, Y. S., Lee, J. H., Yi, H., Won, S. and Chun, J. 2012. Introducing EzTaxon-e: a prokaryotic16S rRNA gene sequence database with phylotypes that represent un ultured species. Int. J. Syst. Evol. Microbiol. 62, 716-721. https://doi.org/10.1099/ijs.0.038075-0
  36. Kim, S. H., Kim, D. W., Park, S. Y., Kim, J. H., Kang, G. H., Kang, H. K., Yu, D. J., Na, J. C. and Lee, S. J. 2008. Effect of dietary Lactobacillus on growth performance, intestinal microflora, development of ileal villi, and intestinal mucosa in broiler chickens. J. Anim. Sci. Technol. 50, 667-676. https://doi.org/10.5187/JAST.2008.50.5.667
  37. Kuda, T., Fujii, T., Saheki, K., Hasegawa, A. and Okuzumi, M. 1992. Effects of brown algae on faecal flora of rats. Nihon Suisan Gakk 58, 307-314. https://doi.org/10.2331/suisan.58.307
  38. Kwon, J. Y., CHeigh, H. S. and Song, Y. O. 2004. Weight reduction and lipid lowering effects of Kimchi lactic acid powder in rats fed high fat diets. Kor. J. Food Sci. Technol. 36, 1014-1019.
  39. Li, W. and Godzik, A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658-1659. https://doi.org/10.1093/bioinformatics/btl158
  40. Louis, P., Young, P., Holtrop, G. and Flint, H. J. 2010. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ. Microbiol. 12, 304-314. https://doi.org/10.1111/j.1462-2920.2009.02066.x
  41. Mokdad, A. H., Bowman, B. A., Ford, E. S., Vinicor, F., Marks, J. S. and Koplan, J. P. 2001. The continuing epidemics of obesity and diabetes in the United States. JAMA 286, 1195-200. https://doi.org/10.1001/jama.286.10.1195
  42. Neyrinck, A. M., Possemiers, S., Druart, C., Wiele, T. V., Backer, F. D., Cani, P. D., Larondelle, Y. and Delzenne, N. M. 2011. Prebiotic Effects of wheat Arabinoxyln related to the increase in Bifidofacteria, Roseburia and Bacteroides/ Prevotella in diet-induced obese mice. PLos One 6, e20944. https://doi.org/10.1371/journal.pone.0020944
  43. Oh, S. I., Sung, J. M. and Lee, K. J. 2014. Physicochemical characteristics and antioxidative effects of barley soybean paste (Doenjang) containing kelp extracts. J. Kor. Soc. Food Sci. Nutr. 43, 1843-1851. https://doi.org/10.3746/jkfn.2014.43.12.1843
  44. Olli, K., Saarinen, M. T., Forssten, S. D., Madetoja, M., Herzig, K. H. and Tiihonen, K. 2016. Independent and combined effects of lactitol, polydextrose, and bacteroides thetaiotaomicron on postprandial metabolism and body weight in rats fed a high-fat diet. Front. Nutr. 3, 15.
  45. Park, J. H., Han, N. S., Yoo, J. Y., Shin, H. K. and Koo, Y. J. 1993. Screening of the foodstuffs influencing the growth of Bifidobacterium spp. and Clostridium perfringens. Kor. J. Food Sci. Technol. 25, 582-588.
  46. Park, Y. H., Kim, J. G., Shin, Y. W., Kim, H. S., Kim, Y. J., Chun, T. H., Kim, S. H. and Hang, K. Y. 2008. Effects of Lactobacillus acidophilus 43121 and a mixture of Lactobacillus casei and Bifidobacterium longum on the serum cholesterol level and fecal sterol excretion in hypercholesterolemia-induced pigs. Biosci. Biotechnol. Biochem. 72, 595-600. https://doi.org/10.1271/bbb.70581
  47. Parveen, B., Pillai, K. K., Tamboli, E. T. and Ahmad, S. 2015. Effect of piperine on pharmacokinetics of sodium valproate in plasma samples of rats using gas chromatography-mass spectrometry method. J. Pharm. Bioallied Sci. 7, 317-320. https://doi.org/10.4103/0975-7406.168036
  48. Pellegrini, S., Sordi, V., Bolla, A. M., Saita, D., Ferrarese, R., Canducci, F., Clementi, M., Invernizzi, F., Mariani, A., Bonfanti, R., Barera, G., Testoni, P. A., Doglioni, C., Bosi, E. and Piemonti, L. 2017. Duodenal mucosa of patients with type 1 diabetes shows distinctive inflammatory profile and microbiota. J. Clin. Endocrinol. Metab. 102, 1468-1477. https://doi.org/10.1210/jc.2016-3222
  49. Qu, W., Yuan, X., Zhao, J., Zhang, Y., Hu, J., Wang, J. and Li, J. 2017. Dietary advanced glycation end products modify gut microbial composition and partially increase colon permeability in rats. Mol. Nutr. Food Res. 61, doi: 10.1002/mnfr. 201700118.
  50. Reilly, P., O'Doherty, J. V., Pierce, K. M., Callan, J. J., O'Sullivan, J. T. and Sweeney, T. 2008. The effects of seaweed extract inclusion on gut morphology, selected intestinal microbiota, nutrient digestibility, volatile fatty acid concentrations and the immune status of the weaned pig. Animal 2, 1465-1473.
  51. Robles-Vera, I., Toral, M., Romero, M., Jimenez, R., Sanchez, M., Perez-Vizcaino, F. and Duarte, J. 2017. Antihypertensive effects of probiotics. Curr. Hypertens. Rep. 19, 26. https://doi.org/10.1007/s11906-017-0723-4
  52. Scher, J. U., Sczesnak, A., Longman, R. S., Segata, N., Ubeda, C., Bielski, C., Rostron, T., Cerundolo, V., Pamer, E. G., Abramson, S. B., Huttenhower, C. and Littman, D. R. 2013. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2, e01202.
  53. Settanni, L. and Corsetti, A. 2008. Application of bacteriocins in vegetable food biopreservation. Int. J. Food Microbiol. 121, 123-138. https://doi.org/10.1016/j.ijfoodmicro.2007.09.001
  54. Shida, K., Makino, K., Morishita, A., Takamizawa, K., Hachimura, S., Ametani, A., Sato, T., Kumagai, Y., Habu, S. and Kaminogawa, S. 1998. Lactobacillus casei inhibits antigen-induced IgE secretion through regulation of cytokine production in murine splenocyte cultures. Int. Arch. Allergy Immunol. 115, 278-287. https://doi.org/10.1159/000069458
  55. Sinh, P., Karimi, A., Devendra, K., Waldroup, P. W., Cho, K. K. and Kwon, Y. M. 2013. Influence of penicillin on microbial diversity of the cecal microbiota in broiler chickens. Poult. Sci. 92, 272-276. https://doi.org/10.3382/ps.2012-02603
  56. Slavin, J. L. 2005. Dietary fiber and body weight. Nutrition 21, 411-418. https://doi.org/10.1016/j.nut.2004.08.018
  57. Son, H. S., Kim, H. S. and Ju, J. S. 1992. Effect of seaweeds intake on the absorption of sodium, calcium, potassium and hypolipidemic mechanism in healthy male subjects. J. Kor. Soc. Food Sci. Nutr. 21, 471-477.
  58. Thomas, G. and Fredrik, B. 2011. Effects of the gut microbiota on obesity and glucose homeostasis. Trends. Endocrinol. Metab. 22, 117-123. https://doi.org/10.1016/j.tem.2011.01.002
  59. 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, S. C. and 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. 10, 1-14.
  60. Turnbaugh, P. J., Backhed, F., Fulton, L. and Gordon, J. I. 2008. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213-223. https://doi.org/10.1016/j.chom.2008.02.015
  61. Turnbaugh, P. J., Ley, R. E., Klein, S. and Gordon, J. I. 2006. An obesityassociated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031. https://doi.org/10.1038/nature05414
  62. Udayappan, S., Manneras-Holm, L., Chaplin-Scott, A., Belzer, C., Herrema, H., Dallinga-Thie, G. M., Duncan, S. H., Stroes, E. S. G., Groen, A. K., Flint, H. J., Backhed, F., de Vos, W. M. and Nieuwdorp, M. 2016. Oral treatment with Eubacterium hallii improves insulin sensitivity in db/db mice. NPJ. Biofilms. Microbiomes 2, 16009. https://doi.org/10.1038/npjbiofilms.2016.9
  63. Wang, J. H., Kim, B. S., Han, K. and Kim, H. 2017. Ephedratreated donor-derived gut microbiota transplantation ameliorates high fat diet-induced obesity in rats. Int. J. Environ. Res. Public Health 14, piiE555. https://doi.org/10.3390/ijerph14060555
  64. World Health Organization. 1997. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ. Tech. Rep. Ser. 1-254.
  65. Wu, M., Wu, Y., Deng, B., Li, J., Cao, H., Qu, Y., Qian, X. and Zhong, G. 2016. Isoliquiritigenin decreases the incidence of colitis-associated colorectal cancer by modulating the intestinal microbiota. Oncotarget 7, 85318-85331.
  66. Wu, Z. X., Li, S. F., Chen, H., Song, J. X., Gao, Y. F., Zhang, F. and Cao, C. F. 2017. The changes of gut microbiota after acute myocardial infarction in rats. PLoS One 12, e0180717. https://doi.org/10.1371/journal.pone.0180717
  67. Yang, T., Owen, J. L., Lightfoot, Y. L., Kladde, M. P. and Mohamadzadeh, M. 2013. Microbiota impact on the epigenetic regulation of colorectal cancer. Trends. Mol. Med. 19, 714-725. https://doi.org/10.1016/j.molmed.2013.08.005
  68. Zhang, X., Wang, H., Yin, P., Fan, H., Sun, L. and Liu, Y. 2017. Flaxseed oil ameliorates alcoholic liver disease via anti-inflammation and modulating gut microbiota in mice. Lipids Health Dis. 16, 44. https://doi.org/10.1186/s12944-017-0431-8