Probiotics’ effect on visceral and subcutaneous adipose tissue: A systematic review of randomized controlled trials
Abstract
Probiotics are shown to alter the microbiota, leading to a favorable environment, in which weight loss and metabolic parameters are improve. However, the results on probiotics' effect on specific types of central adipose tissues, mainly visceral (VAT) and subcutaneous adipose tissue (SAT), are conflicting. Therefore, we conducted a systematic review, aimed to evaluate the effects of probiotics on VAT and SAT. PubMed, SCOPUS, EBSCO, and LILACS databases were searched for studies that investigated the effect of probiotics on VAT and SAT. Fixed effects were used to calculate the pooled difference in means (DM) and 95% confidence intervals (95%CI). Fourteen publications met the inclusion criteria, which consisted of 1523 participants. For VAT, overall, there was a significant decrease (DM = -3.63 cm 2, 95% CI: -5.08 to -2.17, p < 0.001). When stratified by type of probiotic, single Bifidobacterium (DM = -4.49 cm 2, 95% CI:-7.37 to -1.61, p = 0.002) and single Lactobacillus probiotics (DM = -3.84 cm 2, 95% CI:-5.74 to -1.93, p < 0.001) resulted in significant reductions. Mixed probiotics had no effect. For SAT, overall, there was a significant decrease (DM = -2.91 cm 2, 95% CI:-4.82 to -1.01, p = 0.003), and when stratified by type of probiotic, single Lactobacillus (DM = -3.39 cm 2, 95% CI:-5.90 to -0.88, p = 0.008) and mixed probiotics (DM = -5.97 cm 2, 95% CI:-10.32 to -1.62, p = 0.007) resulted in a significant decrease. Single Bifidobacterium probiotics had no effect. Using meta-regression, no association was observed between the total daily probiotic dose and VAT or SAT reduction. This study shows that probiotics have a beneficial effect on central adiposity. Single Lactobacillus-based probiotics reduced VAT and SAT, whereas Bifidobacterium-based probiotics reduce VAT.
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Bias in meta-analysis detected by a simple, graphical test
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) · BMJ · doi:10.1136/bmj.315.7109.629 · Cited by 56,722 · see citing works
Assessing the quality of reports of randomized clinical trials: Is blinding necessary?
Jadad, A. R., Moore, R. A., Carroll, D., Jenkinson, C., Reynolds, D. J. M., Gavaghan, D. J., & McQuay, H. J. (1996) · Controlled Clinical Trials · doi:10.1016/0197-2456(95)00134-4 · Cited by 17,582 · see citing works
Stang, A. (2010) · European Journal of Epidemiology · doi:10.1007/s10654-010-9491-z · Cited by 17,396 · see citing works
Operating characteristics of a rank correlation test for publication bias
Begg, C. B., & Mazumdar, M. (1994) · Biometrics · doi:10.2307/2533446 · Cited by 16,955 · see citing works
Statistical Aspects of the Analysis of Data From Retrospective Studies of Disease
(1959) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/22.4.719 · Cited by 14,689 · cited 1× · see citing works
“0%) was used to calculate the pooled DM and 95%CI [19, 20].”
MethodZhang, Q., Wang, C., Zheng, M., Li, Y., Li, J., Zhang, L., Shang, X., & Yan, C. (2014) · Cerebrovascular Diseases · doi:10.1159/000369778 · Cited by 11,609 · see citing works
The metabolic phenotype in obesity: Fat mass, body fat distribution, and adipose tissue function
Goossens, G. H. (2017) · Obesity Facts · doi:10.1159/000471488 · Cited by 8,481 · see citing works
Dong, Y., Hao, L., Shi, Z., Wang, G., Zhang, Z., & Han, C. (2013) · Urologia Internationalis · doi:10.1159/000351405 · Cited by 4,556 · see citing works
Abdominal obesity and metabolic syndrome
Després, J.-P., & Lemieux, I. (2006) · Nature · doi:10.1038/nature05488 · Cited by 4,354 · see citing works
Rinninella, E., Raoul, P., Cintoni, M., Franceschi, F., Miggiano, G. A. D., Gasbarrini, A., & Mele, M. C. (2019) · Microorganisms · doi:10.3390/microorganisms7010014 · Cited by 3,462 · see citing works
Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome
Wajchenberg, B. L. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.6.0415 · Cited by 2,961 · see citing works
Effects of probiotics, prebiotics, and synbiotics on human health
Markowiak, P., & Śliżewska, K. (2017) · Nutrients · doi:10.3390/nu9091021 · Cited by 2,401 · see citing works
Subcutaneous and visceral adipose tissue: Structural and functional differences
Ibrahim, M. M. (2010) · Obesity Reviews · doi:10.1111/j.1467-789x.2009.00623.x · Cited by 2,238 · see citing works
Stanhope, K. L., Schwarz, J. M., Keim, N. L., Griffen, S. C., Bremer, A. A., Graham, J. L., Hatcher, B., Cox, C. L., Dyachenko, A., Zhang, W., et al. (2009) · Journal of Clinical Investigation · doi:10.1172/jci37385 · Cited by 1,765 · see citing works
Mechanisms of action of probiotics
Plaza-Diaz, J., Ruiz-Ojeda, F. J., Gil-Campos, M., & Gil, A. (2019) · Advances in Nutrition · doi:10.1093/advances/nmy063 · Cited by 1,423 · see citing works
Chronic Adipose Tissue Inflammation Linking Obesity to Insulin Resistance and Type 2 Diabetes
Zatterale, F., Longo, M., Naderi, J., Raciti, G. A., Desiderio, A., Miele, C., & Beguinot, F. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2019.01607 · Cited by 1,180 · see citing works
Chelakkot, C., Choi, Y., Kim, D., Park, H. T., Ghim, J., Kwon, Y., Jeon, J., Kim, M.-S., Jee, Y., Gho, Y. S., et al. (2018) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.282 · Cited by 859 · see citing works
Energy balance and obesity: what are the main drivers?
On behalf of the IARC working group on Energy Balance and Obesity, Romieu, I., Dossus, L., Barquera, S., Blottière, H. M., Franks, P. W., Gunter, M. J., Hwalla, N. C., Hursting, S. D., Leitzmann, M. F., et al. (2017) · Cancer Causes & Control · doi:10.1007/s10552-017-0869-z · Cited by 745 · see citing works
Kadooka, Y., Sato, M., Imaizumi, K., Ogawa, A., Ikuyama, K., Akai, Y., Okano, M., Kagoshima, M., & Tsuchida, T. (2010) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2010.19 · Cited by 700 · see citing works
Health Benefits of Heat-Killed (Tyndallized) Probiotics: An Overview
Piqué, N., Berlanga, M., & Miñana-Galbis, D. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20102534 · Cited by 642 · see citing works
The Inverse of the Freeman – Tukey Double Arcsine Transformation
Miller, J. J. (1978) · The American Statistician · doi:10.1080/00031305.1978.10479283 · Cited by 501 · see citing works
Aldose Reductase, Oxidative Stress, and Diabetic Mellitus
Tang, W. H., Martin, K. A., & Hwa, J. (2012) · Frontiers in Pharmacology · doi:10.3389/fphar.2012.00087 · Cited by 458 · see citing works
Bifidobacterium longum with Fructo-Oligosaccharides in Patients with Non Alcoholic Steatohepatitis
Malaguarnera, M., Vacante, M., Antic, T., Giordano, M., Chisari, G., Acquaviva, R., Mastrojeni, S., Malaguarnera, G., Mistretta, A., Volti, G. L., et al. (2011) · Digestive Diseases and Sciences · doi:10.1007/s10620-011-1887-4 · Cited by 456 · see citing works
Million, M., Angelakis, E., Paul, M., Armougom, F., Leibovici, L., & Raoult, D. (2012) · Microbial Pathogenesis · doi:10.1016/j.micpath.2012.05.007 · Cited by 431 · see citing works
Contribution of Adipose Tissue Inflammation to the Development of Type 2 Diabetes Mellitus
Burhans, M. S., Hagman, D. K., Kuzma, J. N., Schmidt, K. A., & Kratz, M. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170040 · Cited by 427 · see citing works
Aller, R., de Luis, D. A., Izaola, O., Conde, R., Sagrado, M. G., Primo, D., Fuente, B. D. L., & González‐Gallego, J. (2011) · PubMed · Cited by 371 · see citing works
The Relationship Between Gut Microbiota and Weight Gain in Humans
Angelakis, E., Armougom, F., Million, M., & Raoult, D. (2011) · Future Microbiology · doi:10.2217/fmb.11.142 · Cited by 357 · see citing works
Abraham, T. M., Pedley, A., Massaro, J. M., Hoffmann, U., & Fox, C. S. (2015) · Circulation · doi:10.1161/circulationaha.114.015000 · Cited by 353 · see citing works
Effects of Lactobacillus rhamnosus Strain GG in Pediatric Obesity‐related Liver Disease
Vajro, P., Mandato, C., Licenziati, M. R., Franzese, A., Vitale, D. F., Lenta, S., Caropreso, M., Vallone, G., & Meli, R. (2011) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e31821f9b85 · Cited by 343 · see citing works
Probiotics, prebiotics, synbiotics and insulin sensitivity
Kim, Y. A., Keogh, J. B., & Clifton, P. M. (2017) · Nutrition Research Reviews · doi:10.1017/s095442241700018x · Cited by 341 · see citing works
Probiotics for Gastrointestinal Conditions: A Summary of the Evidence.
Wilkins, T., & Sequoia, J. (2017) · PubMed · Cited by 328 · see citing works
Liver Abscess Due to aLactobacillus rhamnosusStrain Indistinguishable fromL. rhamnosusStrain GG
Rautio, M., Jousimies-Somer, H. R., Kauma, H., Pietarinen, I., Saxelin, M., Tynkkynen, S., & Koskela, M. (1999) · Clinical Infectious Diseases · doi:10.1086/514766 · Cited by 327 · see citing works
Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases
Agerholm-Larsen, L., Raben, A., Haulrik, N., Hansen, A., Manders, M., & Astrup, A. V. (2000) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1600937 · Cited by 319 · see citing works
Maurovich‐Horvat, P., Massaro, J. M., Fox, C. S., Moselewski, F., O’Donnell, C. J., & Hoffmann, U. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803454 · Cited by 299 · see citing works
Probiotics: Properties, Examples, and Specific ApplicationsPreprint
Behnsen, J., Deriu, E., Sassone‐Corsi, M., & Raffatellu, M. (2013) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a010074 · Cited by 293 · see citing works
Borgeraas, H., Johnson, L. K., Skattebu, J., Hertel, J. K., & Hjelmesæth, J. (2018) · Obesity Reviews · doi:10.1111/obr.12626 · Cited by 278 · see citing works
Mobini, R., Tremaroli, V., Ståhlman, M., Karlsson, F. H., Levin, M., Ljungberg, M., Sohlin, M. C., Forslund, H. B., Perkins, R., Bäckhed, F., et al. (2016) · Diabetes Obesity and Metabolism · doi:10.1111/dom.12861 · Cited by 266 · see citing works
A review of dose-responses of probiotics in human studies
Ouwehand, A. C. (2016) · Beneficial Microbes · doi:10.3920/bm2016.0140 · Cited by 233 · see citing works
Kadooka, Y., Sato, M., Ogawa, A., Miyoshi, M., Uenishi, H., Ogawa, H., Ikuyama, K., Kagoshima, M., & Tsuchida, T. (2013) · British Journal Of Nutrition · doi:10.1017/s0007114513001037 · Cited by 232 · see citing works
Canfora, E. E., van der Beek, C. M., Hermes, G. D. A., Goossens, G. H., Jocken, J. W. E., Holst, J. J., van Eijk, H. M. H., Venema, K., Smidt, H., Zoetendal, E. G., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.03.051 · Cited by 227 · see citing works
Islam, S. U. (2016) · Medicine · doi:10.1097/md.0000000000002658 · Cited by 220 · see citing works
Ruan, Y., Sun, J. M., He, J., Chen, F., Chen, R., & Chen, H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132121 · Cited by 214 · see citing works
Choi, J. H., Moon, C. M., Shin, T.-S., Kim, E. K., McDowell, A., Jo, M. K., Joo, Y. H., Kim, S., Jung, H., Shim, K., et al. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0359-3 · Cited by 209 · see citing works
Ahn, S. B., Jun, D. W., Kang, B.-K., Lim, J. H., Lim, S., & Chung, M.-J. (2019) · Scientific Reports · doi:10.1038/s41598-019-42059-3 · Cited by 206 · see citing works
Pedret, A., Valls, R. M., Calderón-Pérez, L., Llauradó, E., Companys, J., Pla‐Pagà, L., Moragas, A., Martín‐Luján, F., Ortega, Y., Giralt, M., et al. (2018) · International Journal of Obesity · doi:10.1038/s41366-018-0220-0 · Cited by 202 · see citing works
Szulińska, M., Łoniewski, I., van Hemert, S., Sobieska, M., & Bogdański, P. (2018) · Nutrients · doi:10.3390/nu10060773 · Cited by 191 · see citing works
Kim, J., Yun, J. M., Kim, M. K., Kwon, O., & Cho, B. (2018) · Journal of Medicinal Food · doi:10.1089/jmf.2017.3937 · Cited by 182 · see citing works
Zhang, Y., Li, L., Guo, C., Mu, D., Feng, B., Zuo, X., & Li, Y. (2016) · BMC Gastroenterology · doi:10.1186/s12876-016-0470-z · Cited by 180 · see citing works
John, G. K., Wang, L., Nanavati, J., Twose, C., Singh, R., & Mullin, G. E. (2018) · Genes · doi:10.3390/genes9030167 · Cited by 143 · see citing works
Jung, S.-P., Lee, K.-M., Kang, J.-H., Yun, S.-I., Park, H.-O., Moon, Y., & Kim, J.-Y. (2013) · Korean Journal of Family Medicine · doi:10.4082/kjfm.2013.34.2.80 · Cited by 140 · see citing works
Tong, L., Hao, H., Zhang, X., Zhang, Z., Lv, Y., Zhang, L., & Yi, H. (2020) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201901251 · Cited by 139 · see citing works
DiNicolantonio, J. J., Mehta, V., Onkaramurthy, N. J., & O’Keefe, J. H. (2017) · Progress in Cardiovascular Diseases · doi:10.1016/j.pcad.2017.12.001 · Cited by 132 · see citing works
MINAMI, J., Iwabuchi, N., Tanaka, M., Yamauchi, K., Xiao, J., Abe, F., & Sakane, N. (2018) · Bioscience of Microbiota Food and Health · doi:10.12938/bmfh.18-001 · Cited by 123 · see citing works
Anwar, M. A., Kralj, S., Piqué, A. V., Leemhuis, H., van der Maarel, M. J. E. C., & Dijkhuizen, L. (2010) · Microbiology · doi:10.1099/mic.0.036616-0 · Cited by 121 · see citing works
Higashikawa, F., Noda, M., Awaya, T., Danshiitsoodol, N., Matoba, Y., Kumagai, T., & Sugiyama, M. (2016) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2016.17 · Cited by 120 · see citing works
Measurement of visceral adipose tissue by DXA combined with anthropometry in obese humans
Bertin, É., Marcus, C. D., Ruiz, J., Eschard, J.-P., & Leuténegger, M. (2000) · International Journal of Obesity · doi:10.1038/sj.ijo.0801121 · Cited by 110 · see citing works
Zhao, X., Higashikawa, F., Noda, M., Kawamura, Y., Matoba, Y., Kumagai, T., & Sugiyama, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030696 · Cited by 106 · see citing works
Díez-Sainz, E., Milagro, F. I., Riezu‐Boj, J. I., & Lorente‐Cebrián, S. (2021) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-021-00837-6 · Cited by 104 · see citing works
Obesity-Related Digestive Diseases and Their Pathophysiology
Nam, S. Y. (2016) · Gut and Liver · doi:10.5009/gnl15557 · Cited by 102 · see citing works
Is It Time to Use Probiotics to Prevent or Treat Obesity?
Brusaferro, A., Cozzali, R., Orabona, C., Biscarini, A., Farinelli, E., Cavalli, E., Grohmann, U., Principi, N., & Esposito, S. (2018) · Nutrients · doi:10.3390/nu10111613 · Cited by 102 · see citing works
Song, E., Han, K., Lim, T.-J., Lim, S., Chung, M.-J., Nam, M. H., Kim, H., & Nam, Y. (2020) · The EPMA Journal · doi:10.1007/s13167-020-00198-y · Cited by 96 · see citing works
Effects of probiotics on nonalcoholic fatty liver disease: a systematic review and meta-analysis
Tang, Y., Huang, J., Zhang, W. Y., Qin, S., Yang, Y. X., Ren, H., Yang, Q.-B., & Hu, H. (2019) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756284819878046 · Cited by 85 · see citing works
Jones, R. B., Alderete, T. L., Martin, A., Geary, B. A., Hwang, D., Palmer, S. L., & Goran, M. I. (2018) · Pediatric Obesity · doi:10.1111/ijpo.12273 · Cited by 83 · see citing works
Jung, S., Lee, Y. J., Kim, M., Kim, M., Kwak, J. H., Lee, J., Ahn, Y.-T., Jae-Hun, S., & Lee, J. H. (2015) · Journal of Functional Foods · doi:10.1016/j.jff.2015.10.006 · Cited by 77 · see citing works
Visceral fat and insulin resistance - what we know?
Janochova, K., Haluzik, M., & Bužga, M. (2018) · Biomedical Papers · doi:10.5507/bp.2018.062 · Cited by 72 · see citing works
Kim, M., Kim, M., Kang, M., Yoo, H. J., Kim, M. S., Ahn, Y.-T., Sim, J.-H., Jee, S. H., & Lee, J. H. (2017) · Food & Function · doi:10.1039/c6fo00993j · Cited by 67 · see citing works
Pisanu, S., Palmas, V., Madau, V., Casula, E., Deledda, A., Cusano, R., Uva, P., Vascellari, S., Boi, F., Loviselli, A., et al. (2020) · Nutrients · doi:10.3390/nu12092707 · Cited by 66 · see citing works
Leyrolle, Q., Cserjési, R., Mulders, M. D. G. H., Zamariola, G., Hiel, S., Gianfrancesco, M. A., Portheault, D., Amadieu, C., Bindels, L. B., Leclercq, S., et al. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.01.014 · Cited by 66 · see citing works
Le Barz, M., Daniel, N., Varin, T. V., Naimi, S., Demers‐Mathieu, V., Pilon, G., Audy, J., Laurin, É., Roy, D., Urdaci, M. C., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201801672r · Cited by 63 · see citing works
Gut microbiota is associated with adiposity markers and probiotics may impact specific genera
Gomes, A. C., Hoffmann, C., & Mota, J. F. (2019) · European Journal of Nutrition · doi:10.1007/s00394-019-02034-0 · Cited by 62 · see citing works
Takahashi, S., Anzawa, D., Kazuyo, T., Ishizuka, A., Mawatari, T., Kamikado, K., Haruhi, S., & Nishijima, T. (2016) · Bioscience of Microbiota Food and Health · doi:10.12938/bmfh.2016-002 · Cited by 61 · see citing works
Ruscica, M., Pavanello, C., Gandini, S., Macchi, C., Botta, M., Dall’Orto, D., Puppo, M. D., Bertolotti, M., Bosisio, R., Mombelli, G. G., et al. (2019) · Nutrition Journal · doi:10.1186/s12937-019-0438-2 · Cited by 60 · see citing works
Wang, X., Rao, H., Liu, F., Wei, L., Li, H., & Wu, C. (2021) · Cells · doi:10.3390/cells10123300 · Cited by 60 · see citing works
Nakamura, F., Ishida, Y., Aihara, K., Sawada, D., Ashida, N., Sugawara, T., Aoki, Y., Takehara, I., Takano, K., & Fujiwara, S. (2016) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v27.30312 · Cited by 47 · see citing works
Intestine-liver crosstalk in Type 2 Diabetes and non-alcoholic fatty liver disease
Nawrot, M., Peschard, S., Lestavel, S., & Staels, B. (2021) · Metabolism · doi:10.1016/j.metabol.2021.154844 · Cited by 43 · see citing works
Effects of probiotics on nonalcoholic fatty liver disease: a systematic review and meta-analysis
Yang, R., Shang, J., Zhou, Y., Liu, W., Tian, Y., & Shang, H. (2021) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2022.2016391 · Cited by 43 · see citing works
Moon, Y., Baik, S., & Cha, Y. (2014) · Nutrients · doi:10.3390/nu6031016 · Cited by 41 · see citing works
Sugawara, T., Sawada, D., Yanagihara, S., Aoki, Y., Takehara, I., Sugahara, H., Hirota, T., Nakamura, Y., & Ishikawa, S. (2020) · Microorganisms · doi:10.3390/microorganisms8020304 · Cited by 41 · see citing works
Wang, S., Pan, J., Zhang, Z., & Yan, X. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.103955 · Cited by 39 · see citing works
Toshimitsu, T., Gotou, A., Sashihara, T., Furuichi, K., Hachimura, S., Shioya, N., Suzuki, S., & Asami, Y. (2021) · Current Developments in Nutrition · doi:10.1093/cdn/nzab006 · Cited by 37 · see citing works
Smarkusz-Zarzecka, J., Ostrowska, L., Leszczyńska, J., Orywal, K., Cwalina, U., & Pogodziński, D. (2020) · Nutrients · doi:10.3390/nu12123758 · Cited by 35 · see citing works
The Effect of Diet or Exercise on Visceral Adipose Tissue in Overweight Youth
Vissers, D. K., Hens, W., Hansen, D., & Taeymans, J. (2016) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000888 · Cited by 33 · see citing works
Asgharian, A., Mohammadi, V., Gholi, Z., Esmaillzade, A., Feizi, A., & Askari, G. (2017) · Iranian Red Crescent Medical Journal · doi:10.5812/ircmj.42902 · Cited by 30 · see citing works
Pan, R., Xu, T., Bai, J., Xia, S., Liu, Q., Li, J., Xiao, X., & Dong, Y. (2020) · Journal of Food Biochemistry · doi:10.1111/jfbc.13471 · Cited by 27 · see citing works
Smith‐Ryan, A. E., Mock, M. G., Trexler, E. T., Hirsch, K. R., & Blue, M. N. M. (2018) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2018-0645 · Cited by 22 · see citing works
Artene, D., Bordea, C. I., & Blidaru, A. (2017) · Chirurgia · doi:10.21614/chirurgia.112.4.457 · Cited by 21 · see citing works
Banach, K., Glibowski, P., & Jedut, P. (2020) · Applied Sciences · doi:10.3390/app10175830 · Cited by 18 · see citing works
Matsuoka, R., Kamachi, K., Usuda, M., Wang, W., Masuda, Y., Kunou, M., Tanaka, A., & Utsunomiya, K. (2017) · Lipids in Health and Disease · doi:10.1186/s12944-017-0631-2 · Cited by 17 · see citing works
Zhang, Q., Kim, J., Kim, Y., & Kim, W. (2020) · Journal of Dairy Science · doi:10.3168/jds.2020-18681 · Cited by 15 · see citing works
Factors Associated with Visceral Fat Loss in Response to a Multifaceted Weight Loss Intervention
Liu, F., Flatt, S. W., Nichols, J. F., Pakiz, B., Barkai, H., Wing, D. R., Heath, D. D., & Rock, C. L. (2017) · Journal of Obesity & Weight loss Therapy · doi:10.4172/2165-7904.1000346 · Cited by 11 · see citing works
Distribution of Abdominal Obesity and Fitness Level in Overweight and Obese Korean Adults
Kim, S., Kim, J. Y., Lee, D., Lee, H. S., Lee, J., & Jeon, J. Y. (2014) · International Journal of Endocrinology · doi:10.1155/2014/854392 · Cited by 7 · see citing works
Glycemic index of boiled BARLEYmax® in healthy Japanese subjects
Nomura, N., Miyoshi, T., Hamada, Y., & Kitazono, E. (2020) · Journal of Cereal Science · doi:10.1016/j.jcs.2020.102959 · Cited by 6 · see citing works
Artene, D., Bordea, C. I., & Blidaru, A. (2017) · Romanian Medical Journal · doi:10.37897/rmj.2017.2.6 · Cited by 1 · see citing works
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Cited by
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Accounting for the health risk of probiotics
Liu, X., Zhao, H., & Wong, A. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e27908 · Cited by 44 · see citing works
Current Concepts in Probiotic Safety and Efficacy
Churin, A. A., Sokolyanskaya, L. O., Lukina, A. P., & Karnachuk, O. V. (2026) · Nutrients · doi:10.3390/nu18040696 · Cited by 31 · see citing works
“Conclusions were not universally positive, and some studies even reported unexpected side effects [87,108].”
Riveros, N., García-Corredor, L., Martinez-Solarte, M., & Clavijo, A. ́. G. (2024) · Journal of the American Nutrition Association · doi:10.1080/27697061.2024.2320192 · Cited by 15 · see citing works
Danielsson, P., Putri, R. R., Marcus, C., & Hagman, E. (2023) · Scientific Reports · doi:10.1038/s41598-023-45395-7 · Cited by 12 · see citing works
Vazquez-Marroquin, G., Ochoa-Précoma, R., Porchia, L. M., Pérez-Fuentes, R., Nicolás‐Toledo, L., Rodríguez‐Antolín, J., & González-Mejía, M. E. (2023) · Journal of the Academy of Nutrition and Dietetics · doi:10.1016/j.jand.2023.01.006 · Cited by 6 · see citing works
Self-citationLi, N., Zhu, Z., Wu, S., Gong, D., Day, R., Vijayakumar, V., Yu, X., Chen, Q., Feng, Y., Wang, Q., et al. (2025) · Clinical Nutrition · doi:10.1016/j.clnu.2025.106560 · Cited by 4 · see citing works
Shobako, N., Shimada, H., Yamato, T., Nakazeko, T., Hirano, Y., Nakamura, F., & Honda, K. (2024) · Nutrients · doi:10.3390/nu16183202 · Cited by 4 · see citing works
Pontes‐Silva, A., Ковалева, О. Н., Gadzhiakhmedova, A. N., Luchina, A. M., Sinelnikov, M. Y., Maslennikov, R. V., Musaeva, A. M., Zharova, N. V., Zharikova, T. M., & Zharikov, Y. O. (2023) · Revista da Associação Médica Brasileira · doi:10.1590/1806-9282.20230721 · Cited by 1 · see citing works
Susmiati, S., Melia, S., Khairina, I., & Tofrizal, A. (2025) · Research Journal of Pharmacy and Technology · doi:10.52711/0974-360x.2025.00015
Luo, Y., Li, J., Wu, S., Ren, L., Jia, W., Yang, M., Ouyang, D., Li, Y., He, F., & Cheng, R. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5242629
Microbiome and Diseases: Metabolic Disorders
Clavel, T., & Ecker, J. (2026) · Springer eBooks · doi:10.1007/978-3-032-26410-7_16
- Authors
- Porchia, L. M., Vazquez-Marroquin, G., Ochoa-Précoma, R., Pérez-Fuentes, R., & Gonzalez-Mejia, M. E.
- Affiliations
- Mexican Social Security Institute (MX)
- Universidad Autónoma de Tlaxcala (MX)
- Benemérita Universidad Autónoma de Puebla (MX)
- Venue
- European Journal of Clinical Nutrition
- Published
- 2022-04-13
- Volume
- 76
- Issue
- 12
- Pages
- 1646-1656
- ISSN
- 0954-3007 (ISSN-L)
- 1476-5640
- OpenAlex
- W4223419578
- Cited by
- 10
- References
- 94
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 3 · 2023: 3
- FWCI
- 0.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Clinical Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Programa para el Desarrollo Profesional Docente (CA-160 FACMED) Vicerrectorıa de Investigacion, Benemerita Universidad Autonoma de Puebla, Mexico (GOMM-SAL21-G).
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Keywords
- probiotics, Bifidobacterium, subcutaneous adipose tissue, visceral adipose tissue, abdominal obesity, gut microbiota, weight loss, probiotic dosage, Lactobacillus
- MeSH terms
- Adipose Tissue, Humans, Randomized Controlled Trials as Topic, Probiotics, Subcutaneous Fat, Intra-Abdominal Fat
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