Potential Role of Probiotics for Inflammaging: A Narrative Review
Abstract
:1. Introduction
2. Materials and Methods
3. Results
Reference | Study Sample (Age, n. of Subjects Enrolled) | Inclusion Criteria | Probiotic and Placebo Characteristics and Dosage | Duration of Administration and Follow Up | Effect on Inflammatory Markers |
---|---|---|---|---|---|
De Simone et al. (1992) | Institutionalized older. Mean age 76 years; n = 25 subjects enrolled (n = 15 intervention vs. n = 10 control). | Written informed consent from participants, older than 70 years, no overt diseases according to anamnesis and no fever, pain, cough, dysuria, modification of bowel habits etc. | 2 capsules × 4 times/day, containing combined B. bifidum (109 CFU) and L. acidophilus (109 CFU) vs. 2 capsules × 4 times a day of placebo, containing saccarose and gelatin | 4-week intervention | No effect on plasma TNF-α |
Guillemart et al. (2010) | Free-living older. Mean age 76 years (range 69–95); n = 1072 subjects enrolled in the study. | Both gender, ≥70 years, free living, AGGIR score between 5 and 6, vaccination ag. influenza virus at least 14d before inclusion, MMSA score ≥24, BMI between 17 and 25 kg/m2, compliance with a dietary restriction (no fermented dairy products with other probiotics, yoghurts and medication containing probiotics, vitamins, minerals and other nutrients) during 2 previous weeks and throughout the study, written informed consent. | 2 bottles, 100 g each/day, of fermented diary drink containing at least 1010 CFU/100 g of the probiotic strain L. Casei DN-114001 vs. non fermented diary drink | 12-week intervention + 4-week follow up | No effect on blood CRP, IL-1, IL-6, IFNα, IFNβ, IFNγ, IL-8, IL-10, IL-12 or TNF-α < βγ |
Mañe et al. (2011) | Institutionalized older. Mean age 70 years (range 65–84); n = 60 subjects enrolled; n = 20 placebo, n = 20 low dose probiotic, n = 20 high dose probiotic. | Written informed consent, older than 65 years. | 20 g of powdered skilled milk containing 5 × 108 CFU/day of L. plantarum CECT7315/7316 (low probiotic dose) or 5 × 109 CFU/day of L. plantarum CECT7315/7316 (high probiotic dose) or 20 g of powdered skilled milk (placebo) | 12-week intervention + 12 week follow up | TGF-β decreased (value not given) independent from probiotic dosage |
Moro-García et al. (2013) | Free-living older. Mean age 70 years (range 65–90); n = 61 subjects enrolled. | Older than 65 years, treatment in determined Spanish health centers, written informed consent. | 3 capsules/day containing at least 3 × 107 L. delbrueckii subs bulgaricus 8481 vs. placebo capsules with corn starch | 24-week intervention | Plasma IL-8 decreased (value not given), hBD-2 increased (value not given); no effect on IFN-γ, IL- 1β, IL-2, IL-4, IL-5, IL-6, IL-10, IL-12p70, TNF-α |
Dong et al. (2013) | Free-living older. Range 55–74 years; n = 30 subjects enrolled; n = 16 intervention group vs. n = 14 placebo. | Age 55–80 years, BMI 19–30 kg/m2, good general health, written informed consent. | 2 × 65 mL/day probiotic drink containing 6.5 × 109 CFU/bottle L. casei Shirota vs. 130 mL of skimmed milk/day | 4-week intervention + 4 weeks of washout | No effect on blood CRP, IL-10/Il-12 ratio increased for LPS- stimulated PBMC |
Valentini et al. (2015) | Free living healthy older. Mean age 70.1 ± 3.9 years; n = 69 enrolled (n = 35 intervention vs. n = 34 controls). | Healthy individuals aged 65–85 years, BMI 22–30 kg/m2 and Eastern Cooperative Oncology Group Performance Status (ECOG) 0–2, able to use a computer and with access to the internet, by themselves or with help. | RISTOMED personalized diet and 2 capsules/day containing 112 billion lyophilized bacteria consisting of B. infantis DSM 24737, B. longum DSM 24736, B. breve DSM 24732, L. acidophilus DSM 24735, L. delbrückii ssp. bulgaricus DSM 24734, L. paracasei DSM 24733, L. plantarum DSM 24730, and S. thermophilus DSM 24731 vs. RISTOMED personalized diet | 8-week intervention (56 ± 2 days) | No effect on hsCRP |
Nyangale et al. (2015) | Free-living older 65–80 years, n = 17 subjects probiotic period 1, placebo period 2, n = 17 subjects placebo period 1, probiotic period 2. | Age 65–80 years, written informed consent. | 1 capsule/day containing 109 CFU of Bacillus coagulans GBI-36, 6086 (BC30) per day vs. capsules containing microcrystalline cellulose | 2 treatment periods consisting of 4-week intervention separated by 3-week washout period | No effect on IL-10, TNF-α or CRP |
Spaiser et al. (2015) | Free-living healthy older, range 65–80 years; n = 42 subjects enrolled. | Written informed consent | 2 capsules/day containing a powder mixture of L. gasseri KS-13, B. bifidum G9-1, B. longum MM2 for a total of 3 × 109 viable cells / day vs. capsules containing potato starch and silicon dioxide | 3-week intervention and 1-week post intervention for each period of crossover + 5-week washout between the intervention periods | IFN-γ increased after period 1 in intervention and after period 2 in both groups, IFN-γ increased after period 2 in both groups, IL-5 and IL-10 increased with probiotic interventions during both periods |
Lee et al. (2017) | Free-living older. Mean age placebo 65.7 ± 0.56 years, probiotic, 65.7 ± 0.50 years; n = 200 subjects enrolled. | Non diabetic (fasting serum glucose concentration < 126 mg/dL), age > 60 years, white blood cell levels between 4 × 103/µL and 10 × 103/µL, written informed consent. | 1 bottle (120 mL)/day of yogurt containing L. paracasei (L. casei 431®) at 12.0 × 108 CFU/day, B. lactis (BB-12®) at 12.0 × 108 CFU/day and 0.0175% heat-treated L. plantarum (nF1) per day vs. 120 mL of milk | 12-week intervention | IL-12 and IFN-γ increased, no effect on CRP |
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Vollset, S.E.; Goren, E.; Yuan, C.-W.; Cao, J.; E Smith, A.; Hsiao, T.; Bisignano, C.; Azhar, G.S.; Castro, E.; Chalek, J.; et al. Fertility, mortality, migration, and population scenarios for 195 countries and territories from 2017 to 2100: A forecasting analysis for the Global Burden of Disease Study. Lancet 2020, 396, 1285–1306. [Google Scholar] [CrossRef]
- Ferrucci, L.; Fabbri, E. Inflammageing: Chronic inflammation in ageing, cardiovascular disease, and frailty. Nat. Rev. Cardiol. 2018, 15, 505–522. [Google Scholar] [CrossRef]
- Franceschi, C.; Garagnani, P.; Morsiani, C.; Conte, M.; Santoro, A.; Grignolio, A.; Monti, D.; Capri, M.; Salvioli, S. The Continuum of Aging and Age-Related Diseases: Common Mechanisms but Different Rates. Front. Med. 2018, 5, 61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fulop, T.; Larbi, A.; Dupuis, G.; Le Page, A.; Frost, E.H.; Cohen, A.A.; Witkowski, J.M.; Franceschi, C. Immunosenescence and Inflamm-Aging As Two Sides of the Same Coin: Friends or Foes? Front. Immunol. 2018, 8, 1960. [Google Scholar] [CrossRef] [Green Version]
- Franceschi, C.; Bonafè, M. Centenarians as a model for healthy aging. Biochem. Soc. Trans. 2003, 31, 457–461. [Google Scholar] [CrossRef] [PubMed]
- Franceschi, C.; Capri, M.; Monti, D.; Giunta, S.; Olivieri, F.; Sevini, F.; Panourgia, M.P.; Invidia, L.; Celani, L.; Scurti, M.; et al. Inflammaging and anti-inflammaging: A systemic perspective on aging and longevity emerged from studies in humans. Mech. Ageing Dev. 2007, 128, 92–105. [Google Scholar] [CrossRef] [PubMed]
- Minciullo, P.L.; Catalano, A.; Mandraffino, G.; Casciaro, M.; Crucitti, A.; Maltese, G.; Morabito, N.; Lasco, A.; Gangemi, S.; Basile, G. Inflammaging and Anti-Inflammaging: The Role of Cytokines in Extreme Longevity. Arch. Immunol. Ther. Exp. 2016, 64, 111–126. [Google Scholar] [CrossRef] [PubMed]
- Calabrese, V.; Santoro, A.; Monti, D.; Crupi, R.; di Paola, R.; Latteri, S.; Cuzzocrea, S.; Zappia, M.; Giordano, J.; Calabrese, E.J.; et al. Aging and Parkinson’s Disease: Inflammaging, neuroinflammation and biological remodeling as key factors in pathogenesis. Free Radic. Biol. Med. 2018, 115, 80–91. [Google Scholar] [CrossRef]
- Franceschi, C.; Garagnani, P.; Parini, P.; Giuliani, C.; Santoro, A. Inflammaging: A new immune–metabolic viewpoint for age-related diseases. Nat. Rev. Endocrinol. 2018, 14, 576–590. [Google Scholar] [CrossRef]
- Furman, D.; Campisi, J.; Verdin, E.; Carrera-Bastos, P.; Targ, S.; Franceschi, C.; Ferrucci, L.; Gilroy, D.W.; Fasano, A.; Miller, G.W.; et al. Chronic inflammation in the etiology of disease across the life span. Nat. Med. 2019, 25, 1822–1832. [Google Scholar] [CrossRef]
- Franceschi, C.; Campisi, J. Chronic Inflammation (Inflammaging) and Its Potential Contribution to Age-Associated Diseases. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2014, 69 (Suppl. S1), S4–S9. [Google Scholar] [CrossRef]
- Arboleya, S.; Watkins, C.; Stanton, C.; Ross, R.P. Gut Bifidobacteria Populations in Human Health and Aging. Front. Microbiol. 2016, 7, 1204. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Minihane, A.M.; Vinoy, S.; Russell, W.R.; Baka, A.; Roche, H.M.; Tuohy, K.M.; Teeling, J.L.; Blaak, E.E.; Fenech, M.; Vauzour, D.; et al. Low-grade inflammation, diet composition and health: Current research evidence and its translation. Br. J. Nutr. 2015, 114, 999–1012. [Google Scholar] [CrossRef] [Green Version]
- Biagi, E.; Nylund, L.; Candela, M.; Ostan, R.; Bucci, L.; Pini, E.; Nikkïla, J.; Monti, D.; Satokari, R.; Franceschi, C.; et al. Through Ageing, and Beyond: Gut Microbiota and Inflammatory Status in Seniors and Centenarians. PLoS ONE 2010, 5, e10667. [Google Scholar] [CrossRef]
- O’Toole, P.W.; Jeffery, I. Gut microbiota and aging. Science 2015, 350, 1214–1215. [Google Scholar] [CrossRef] [PubMed]
- Bernardi, S.; Del Bo’, C.; Marino, M.; Gargari, G.; Cherubini, A.; Andrés-Lacueva, C.; Liberona, N.H.; Peron, G.; González-Domínguez, R.; Kroon, P.A.; et al. Polyphenols and Intestinal Permeability: Rationale and Future Perspectives. J. Agric. Food Chem. 2019, 68, 1816–1829. [Google Scholar] [CrossRef] [PubMed]
- Del Bo’, C.; Bernardi, S.; Cherubini, A.; Porrini, M.; Gargari, G.; Hidalgo-Liberona, N.; González-Domínguez, R.; Zamora-Ros, R.; Peron, G.; Marino, M.; et al. A polyphenol-rich dietary pattern improves intestinal permeability, evaluated as serum zonulin levels, in older subjects: The MaPLE randomised controlled trial. Clin. Nutr. 2021, 40, 3006–3018. [Google Scholar] [CrossRef] [PubMed]
- Carding, S.; Verbeke, K.; Vipond, D.T.; Corfe, B.M.; Owen, L.J. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis. 2015, 26, 26191. [Google Scholar] [CrossRef]
- Binda, S.; Hill, C.; Johansen, E.; Obis, D.; Pot, B.; Sanders, M.E.; Tremblay, A.; Ouwehand, A.C. Criteria to Qualify Microorganisms as “Probiotic” in Foods and Dietary Supplements. Front. Microbiol. 2020, 11, 1662. [Google Scholar] [CrossRef]
- Kim, S.-K.; Guevarra, R.B.; Kim, Y.-T.; Kwon, J.; Kim, H.; Cho, J.H.; Kim, H.B.; Lee, J.-H. Role of Probiotics in Human Gut Microbiome-Associated Diseases. J. Microbiol. Biotechnol. 2019, 29, 1335–1340. [Google Scholar] [CrossRef]
- Sonnenburg, J.L.; Fischbach, M.A. Community Health Care: Therapeutic Opportunities in the Human Microbiome. Sci. Transl. Med. 2011, 3, 78ps12. [Google Scholar] [CrossRef] [Green Version]
- Hemarajata, P.; Versalovic, J. Effects of probiotics on gut microbiota: Mechanisms of intestinal immunomodulation and neuromodulation. Ther. Adv. Gastroenterol. 2013, 6, 39–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Madsen, K.L. Enhancement of Epithelial Barrier Function by Probiotics. J. Epithel. Biol. Pharmacol. 2012, 5, 55–59. [Google Scholar] [CrossRef] [Green Version]
- Preidis, G.; Versalovic, J. Targeting the Human Microbiome With Antibiotics, Probiotics, and Prebiotics: Gastroenterology Enters the Metagenomics Era. Gastroenterology 2009, 136, 2015–2031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohr, A.E.; Basile, A.; Crawford, M.S.; Sweazea, K.L.; Carpenter, K.C. Probiotic Supplementation Has a Limited Effect on Circulating Immune and Inflammatory Markers in Healthy Adults: A Systematic Review of Randomized Controlled Trials. J. Acad. Nutr. Diet. 2019, 120, 548–564. [Google Scholar] [CrossRef]
- Calder, P.; Bosco, N.; Bourdet-Sicard, R.; Capuron, L.; Delzenne, N.; Doré, J.; Franceschi, C.; Lehtinen, M.J.; Recker, T.; Salvioli, S.; et al. Health relevance of the modification of low grade inflammation in ageing (inflammageing) and the role of nutrition. Ageing Res. Rev. 2017, 40, 95–119. [Google Scholar] [CrossRef]
- Hutchinson, A.; Tingö, L.; Brummer, R. The Potential Effects of Probiotics and ω-3 Fatty Acids on Chronic Low-Grade Inflammation. Nutrients 2020, 12, 2402. [Google Scholar] [CrossRef]
- Gui, Q.; Wang, A.; Zhao, X.; Huang, S.; Tan, Z.; Xiao, C.; Yang, Y. Effects of probiotic supplementation on natural killer cell function in healthy elderly individuals: A meta-analysis of randomized controlled trials. Eur. J. Clin. Nutr. 2020, 74, 1630–1637. [Google Scholar] [CrossRef]
- Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; A Akl, E.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021, 372, n71. [Google Scholar] [CrossRef]
- De Simone, C.; Ciardi, A.; Grassi, A.; Gardini, S.L.; Tzantzoglou, S.; Trinchieri, V.; Moretti, S.; Jirillo, E. Effect of Bifido bacterium bifidum and Lactobacillus acidophiluson gut mucosa and peripheral blood B lymphocytes. Immunopharmacol. Immunotoxicol. 1992, 14, 331–340. [Google Scholar] [CrossRef]
- Guillemard, E.; Tondu, F.; Lacoin, F.; Schrezenmeir, J. Consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114001 reduces the duration of respiratory infections in the elderly in a randomised controlled trial. Br. J. Nutr. 2009, 103, 58–68. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mañé, J.; Pedrosa, E.; Lorén, V.; A Gassull, M.; Espadaler, J.; Cuñé, J.; Audivert, S.; A Bonachera, M.; Cabré, E. A mixture of Lactobacillus plantarum CECT 7315 and CECT 7316 enhances systemic immunity in elderly subjects. A dose-response, double-blind, placebo-controlled, randomized pilot trial. Nutr. Hosp. 2011, 26, 228–235. [Google Scholar] [PubMed]
- Moro-García, M.A.; Alonso-Arias, R.; Baltadjieva, M.; Benítez, C.F.; Barrial, M.A.F.; Ruisánchez, E.D.; Santos, R.A.; Sánchez, M.Á.; Miján, J.S.; López-Larrea, C. Oral supplementation with Lactobacillus delbrueckii subsp. bulgaricus 8481 enhances systemic immunity in elderly subjects. AGE 2013, 35, 1311–1326. [Google Scholar] [CrossRef] [PubMed]
- Dong, H.; Rowland, I.; Thomas, L.; Yaqoob, P. Immunomodulatory effects of a probiotic drink containing Lactobacillus casei Shirota in healthy older volunteers. Eur. J. Nutr. 2013, 52, 1853–1863. [Google Scholar] [CrossRef]
- Valentini, L.; Pinto, A.; Bourdel-Marchasson, I.; Ostan, R.; Brigidi, P.; Turroni, S.; Hrelia, S.; Hrelia, P.; Bereswill, S.; Fischer, A.; et al. Impact of personalized diet and probiotic supplementation on inflammation, nutritional parameters and intestinal microbiota—The “RISTOMED project”: Randomized controlled trial in healthy older people. Clin. Nutr. 2015, 34, 593–602. [Google Scholar] [CrossRef] [Green Version]
- Nyangale, E.P.; Farmer, S.; Cash, H.A.; Keller, D.; Chernoff, D.; Gibson, G.R. Bacillus coagulans GBI-30, 6086 Modulates Faecalibacterium prausnitzii in Older Men and Women. J. Nutr. 2015, 145, 1446–1452. [Google Scholar] [CrossRef] [Green Version]
- Spaiser, S.J.; Culpepper, T.; Nieves, C.; Ukhanova, M.; Mai, V.; Percival, S.S.; Christman, M.C.; Langkamp-Henken, B. Lactobacillus gasseri KS-13, Bifidobacterium bifidum G9-1, and Bifidobacterium longum MM-2 Ingestion Induces a Less Inflammatory Cytokine Profile and a Potentially Beneficial Shift in Gut Microbiota in Older Adults: A Randomized, Double-Blind, Placebo-Controlled, Crossover Study. J. Am. Coll. Nutr. 2015, 34, 459–469. [Google Scholar] [CrossRef]
- Lee, A.; Lee, Y.J.; Yoo, H.J.; Kim, M.; Chang, Y.; Lee, D.S.; Lee, J.H. Consumption of Dairy Yogurt Containing Lactobacillus paracasei ssp. paracasei, Bifidobacterium animalis ssp. lactis and Heat-Treated Lactobacillus plantarum Improves Immune Function Including Natural Killer Cell Activity. Nutrients 2017, 9, 558. [Google Scholar] [CrossRef]
- Tilg, H.; Zmora, N.; Adolph, T.E.; Elinav, E. The intestinal microbiota fuelling metabolic inflammation. Nat. Rev. Immunol. 2020, 20, 40–54. [Google Scholar] [CrossRef]
- Pérez-Zepeda, M.U.; Cherubini, A.; García-Peña, C.; Zengarini, E.; Gutiérrez-Robledo, L.M. Clinical Trials on Aging Research. In Aging Research—Methodological Issues; Springer Science and Business Media LLC: Berlin/Heidelberg, Germany, 2018; pp. 115–127. [Google Scholar]
- Cherubini, A.; Gasperini, B. How to increase the participation of older subjects in research: Good practices and more evidence are needed! Age Ageing 2017, 46, 878–881. [Google Scholar] [CrossRef] [Green Version]
- Ouwehand, A.C. A review of dose-responses of probiotics in human studies. Benef. Microbes 2017, 8, 143–151. [Google Scholar] [CrossRef] [PubMed]
- Ministero Della Salute. Direzione Generale per L’igiene e la Sicurezza Degli Alimenti e la Nutrizione-Ufficio 4. In Linee Guida su Probiotici e Prebiotici, Roma, Revisione Marzo; 2018. Available online: https://www.salute.gov.it/imgs/C_17_pubblicazioni_1016_allegato.pdf (accessed on 23 August 2021).
- Foligne, B.; Zoumpopoulou, G.; Dewulf, J.; Ben Younes, A.; Chareyre, F.; Sirard, J.-C.; Pot, B.; Grangette, C. A Key Role of Dendritic Cells in Probiotic Functionality. PLoS ONE 2007, 2, e313. [Google Scholar] [CrossRef] [PubMed]
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Jukic Peladic, N.; Dell’Aquila, G.; Carrieri, B.; Maggio, M.; Cherubini, A.; Orlandoni, P. Potential Role of Probiotics for Inflammaging: A Narrative Review. Nutrients 2021, 13, 2919. https://doi.org/10.3390/nu13092919
Jukic Peladic N, Dell’Aquila G, Carrieri B, Maggio M, Cherubini A, Orlandoni P. Potential Role of Probiotics for Inflammaging: A Narrative Review. Nutrients. 2021; 13(9):2919. https://doi.org/10.3390/nu13092919
Chicago/Turabian StyleJukic Peladic, Nikolina, Giuseppina Dell’Aquila, Barbara Carrieri, Marcello Maggio, Antonio Cherubini, and Paolo Orlandoni. 2021. "Potential Role of Probiotics for Inflammaging: A Narrative Review" Nutrients 13, no. 9: 2919. https://doi.org/10.3390/nu13092919
APA StyleJukic Peladic, N., Dell’Aquila, G., Carrieri, B., Maggio, M., Cherubini, A., & Orlandoni, P. (2021). Potential Role of Probiotics for Inflammaging: A Narrative Review. Nutrients, 13(9), 2919. https://doi.org/10.3390/nu13092919