Overview of human intervention studies evaluating the impact of the mediterranean diet on markers of DNA damage

Nutrients

Volumn 11, Issue 2, 2019, Pages

  Del Bo’, Cristian ^a   Marino, Mirko ^a   Martini, Daniela ^b   Tucci, Massimiliano ^a   Ciappellano, Salvatore ^a   Riso, Patrizia ^a   Porrini, Marisa ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF PARMA   (Italy)

Author keywords

Dietary intervention study; DNA damage; DNA repair; Mediterranean diet; Telomere length

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; BIOLOGICAL MARKER; OLIVE OIL; PHYTOCHEMICAL;

ALCOHOL CONSUMPTION; BODY MASS; CHRONIC DISEASE; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION; HUMAN; INTERVENTION STUDY; MEDITERRANEAN DIET; META ANALYSIS (TOPIC); OXIDATIVE STRESS; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK FACTOR; SCREENING;

DIET, MEDITERRANEAN; DNA DAMAGE; HUMANS; OXIDATIVE STRESS; PHYTOCHEMICALS;

EID: 85061857269     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu11020391     Document Type: Review

References (68)

1. Thanan, R.; Oikawa, S.; Hiraku, Y.; Ohnishi, S.; Ma, N.; Pinlaor, S.; Yongvanit, P.; Kawanishi, S.; Murata, M. Oxidative stress and its significant roles in neurodegenerative diseases and cancer. Int. J. Mol. Sci. 2014, 16, 193–217. [CrossRef] [PubMed]
2. Mahat, R.K.; Singh, N.; Gupta, A.; Rathore, V. Oxidative DNA damage and carotid intima media thickness as predictors of cardiovascular disease in pre-diabetic subjects. J. Cardiovasc. Dev. Dis. 2018, 5, 15. [CrossRef] [PubMed]
3. Basu, A.K. DNA damage, mutagenesis and cancer. Int. J. Mol. Sci. 2018, 19, 970. [CrossRef] [PubMed]
4. Blasiak, J.; Arabski, M.; Krupa, R.; Wozniak, K.; Zadrozny, M.; Kasznicki, J.; Zurawska, M.; Drzewoski, J. DNA damage and repair in type 2 diabetes mellitus. Mutat. Res. 2004, 554, 297–304. [CrossRef] [PubMed]
5. Coluzzi, E.; Colamartino, M.; Cozzi, R.; Leone, S.; Meneghini, C.; O’Callaghan, N.; Sgura, A. Oxidative stress induces persistent telomeric DNA damage responsible for nuclear morphology change in mammalian cells. PLoS ONE 2014, 9, e110963. [CrossRef] [PubMed]
6. Prasad, K.N.; Wu, M.; Bondy, S.C. Telomere shortening during aging: Attenuation by antioxidants and anti-inflammatory agents. Mech. Ageing Dev. 2017, 164, 61–66. [CrossRef] [PubMed]
7. Giovannelli, L.; Saieva, C.; Masala, G.; Testa, G.; Salvini, S.; Pitozzi, V.; Riboli, E.; Dolara, P.; Palli, D. Nutritional and lifestyle determinants of DNA oxidative damage: A study in a Mediterranean population. Carcinogenesis 2002, 23, 1483–1489. [CrossRef] [PubMed]
8. Fenech, M.; Bonassi, S. The effect of age, gender, diet and lifestyle on DNA damage measured using micronucleus frequency in human peripheral blood lymphocytes. Mutagenesis 2011, 26, 43–49. [CrossRef] [PubMed]
9. Prado, R.P.; dos Santos, B.F.; Pinto, C.L.; de Assis, K.R.; Salvadori, D.M.; Ladeira, M.S. Influence of diet on oxidative DNA damage, uracil misincorporation and DNA repair capability. Mutagenesis 2010, 25, 483–487. [CrossRef]
10. Freitas-Simoes, T.M.; Ros, E.; Sala-Vila, A. Nutrients, foods, dietary patterns and telomere length: Update of epidemiological studies and randomized trials. Metabolism 2016, 65, 406–415. [CrossRef]
11. Riso, P.; Pinder, A.; Santangelo, A.; Porrini, M. Does tomato consumption effectively increase the resistance of lymphocyte DNA to oxidative damage? Am. J. Clin. Nutr. 1999, 69, 712–718. [CrossRef] [PubMed]
12. Chen, L.; Stacewicz-Sapuntzakis, M.; Duncan, C.; Sharifi, R.; Ghosh, L.; van Breemen, R.; Ashton, D.; Bowen, P.E. Oxidative DNA damage in prostate cancer patients consuming tomato sauce-based entrees as a whole-food intervention. J. Natl. Cancer Inst. 2001, 93, 1872–1879. [CrossRef]
13. Riso, P.; Martini, D.; Møller, P.; Loft, S.; Bonacina, G.; Moro, M.; Porrini, M. DNA damage and repair activity after broccoli intake in young healthy smokers. Mutagenesis 2010, 25, 595–602. [CrossRef] [PubMed]
14. Riso, P.; Martini, D.; Visioli, F.; Martinetti, A.; Porrini, M. Effect of broccoli intake on markers related to oxidative stress and cancer risk in healthy smokers and nonsmokers. Nutr. Cancer 2009, 61, 232–237. [CrossRef] [PubMed]
15. Porrini, M.; Riso, P.; Oriani, G. Spinach and tomato consumption increases lymphocyte DNA resistance to oxidative stress but this is not related to cell carotenoid concentrations. Eur. J. Nutr. 2002, 41, 95–100. [CrossRef] [PubMed]
16. Moser, B.; Szekeres, T.; Bieglmayer, C.; Wagner, K.H.; Mišík, M.; Kundi, M.; Zakerska, O.; Nersesyan, A.; Kager, N.; Zahrl, J.; et al. Impact of spinach consumption on DNA stability in peripheral lymphocytes and on biochemical blood parameters: Results of a human intervention trial. Eur. J. Nutr. 2011, 50, 587–589. [CrossRef] [PubMed]
17. Riso, P.; Klimis-Zacas, D.; Del Bo’, C.; Martini, D.; Campolo, J.; Vendrame, S.; Møller, P.; Loft, S.; De Maria, R.; Porrini, M. Effect of a wild blueberry (Vaccinium angustifolium) drink intervention on markers of oxidative stress, inflammation and endothelial function in humans with cardiovascular risk factors. Eur. J. Nutr. 2013, 52, 949–961. [CrossRef] [PubMed]
18. Del Bo’, C.; Riso, P.; Campolo, J.; Møller, P.; Loft, S.; Klimis-Zacas, D.; Brambilla, A.; Rizzolo, A.; Porrini, M. A single portion of blueberry (Vaccinium corymbosum L) improves protection against DNA damage but not vascular function in healthy male volunteers. Nutr. Res. 2013, 33, 220–227. [CrossRef] [PubMed]
19. Guarnieri, S.; Riso, P.; Porrini, M. Orange juice vs vitamin C: Effect on hydrogen peroxide-induced DNA damage in mononuclear blood cells. Br. J. Nutr. 2007, 97, 639–643. [CrossRef]
20. Rangel-Huerta, O.D.; Aguilera, C.M.; Martin, M.V.; Soto, M.J.; Rico, M.C.; Vallejo, F.; Tomas-Barberan, F.; Perez-de-la-Cruz, A.J.; Gil, A.; Mesa, M.D. Normal or high polyphenol concentration in orange juice affects antioxidant activity, blood pressure, and body weight in obese or overweight adults. J. Nutr. 2015, 145, 1808–1816. [CrossRef]
21. Guaraldi, F.; Deon, V.; Del Bo’, C.; Vendrame, S.; Porrini, M.; Riso, P.; Guardamagna, O. Effect of short-term hazelnut consumption on DNA damage and oxidized LDL in children and adolescents with primary hyperlipidemia: A randomized controlled trial. J. Nutr. Biochem. 2018, 57, 206–211. [CrossRef] [PubMed]
22. López-Uriarte, P.; Nogués, R.; Saez, G.; Bulló, M.; Romeu, M.; Masana, L.; Tormos, C.; Casas-Agustench, P.; Salas-Salvadó, J. Effect of nut consumption on oxidative stress and the endothelial function in metabolic syndrome. Clin. Nutr. 2010, 29, 373–380. [CrossRef]
23. Erba, D.; Riso, P.; Bordoni, A.; Foti, P.; Biagi, P.L.; Testolin, G. Effectiveness of moderate green tea consumption on antioxidative status and plasma lipid profile in humans. J. Nutr. Biochem. 2005, 16, 144–149. [CrossRef] [PubMed]
24. Ho, C.K.; Choi, S.W.; Siu, P.M.; Benzie, I.F. Effects of single dose and regular intake of green tea (Camellia sinensis) on DNA damage, DNA repair, and heme oxygenase-1 expression in a randomized controlled human supplementation study. Mol. Nutr. Food Res. 2014, 58, 1379–1383. [CrossRef] [PubMed]
25. Bakuradze, T.; Lang, R.; Hofmann, T.; Schipp, D.; Galan, J.; Eisenbrand, G.; Richling, E. Coffee consumption rapidly reduces background DNA strand breaks in healthy humans: Results of a short-term repeated uptake intervention study. Mol. Nutr. Food Res. 2016, 60, 682–686. [CrossRef] [PubMed]
26. Bakuradze, T.; Lang, R.; Hofmann, T.; Eisenbrand, G.; Schipp, D.; Galan, J.; Richling, E. Consumption of a dark roast coffee decreases the level of spontaneous DNA strand breaks: A randomized controlled trial. Eur. J. Nutr. 2015, 54, 149–156. [CrossRef] [PubMed]
27. Kiokias, S.; Proestos, C.; Oreopoulou, V. Effect of natural food antioxidants against LDL and DNA oxidative changes. Antioxidants 2018, 7, 133. [CrossRef] [PubMed]
28. Azqueta, A.; Collins, A. Polyphenols and DNA damage: A mixed blessing. Nutrients 2016, 8, 785. [CrossRef] [PubMed]
29. Willett, W.C.; Sacks, F.; Trichopoulou, A.; Drescher, G.; Ferro-Luzzi, A.; Helsing, E.; Trichopoulos, D. Mediterranean diet pyramid: A cultural model for healthy eating. Am. J. Clin. Nutr. 1995, 61 (Suppl. 6), S1402–S1406. [CrossRef] [PubMed]
30. Bach-Faig, A.; Berry, E.M.; Lairon, D.; Reguant, J.; Trichopoulou, A.; Dernini, S.; Medina, F.X.; Battino, M.; Belahsen, R.; Miranda, G.; et al. Mediterranean Diet Foundation Expert Group. Mediterranean diet pyramid today. Science and cultural updates. Public Health Nutr. 2011, 14, 2274–2284. [CrossRef] [PubMed]
31. Koloverou, E.; Panagiotakos, D.B.; Pitsavos, C.; Chrysohoou, C.; Georgousopoulou, E.N.; Grekas, A.; Christou, A.; Chatzigeorgiou, M.; Skoumas, I.; Tousoulis, D.; et al. ATTICA Study Group. Adherence to Mediterranean diet and 10-year incidence (2002-2012) of diabetes: Correlations with inflammatory and oxidative stress biomarkers in the ATTICA cohort study. Diabetes Metab. Res. Rev. 2016, 32, 73–81. [CrossRef] [PubMed]
32. Dinu, M.; Pagliai, G.; Casini, A.; Sofi, F. Mediterranean diet and multiple health outcomes: An umbrella review of meta-analyses of observational studies and randomised trials. Eur. J. Clin. Nutr. 2018, 72, 30–43. [CrossRef] [PubMed]
33. Bonaccio, M.; Di Castelnuovo, A.; Costanzo, S.; Gialluisi, A.; Persichillo, M.; Cerletti, C.; Donati, M.B.; de Gaetano, G.; Iacoviello, L. Mediterranean diet and mortality in the elderly: A prospective cohort study and a meta-analysis. Br. J. Nutr. 2018, 120, 841–854. [CrossRef] [PubMed]
34. Buil-Cosiales, P.; Toledo, E.; Salas-Salvadó, J.; Zazpe, I.; Farràs, M.; Basterra-Gortari, F.J.; Diez-Espino, J.; Estruch, R.; Corella, D.; Ros, E.; et al. Association between dietary fibre intake and fruit, vegetable or whole-grain consumption and the risk of CVD: Results from the PREvención con DIeta MEDiterránea (PREDIMED) trial. Br. J. Nutr. 2016, 116, 534–546. [CrossRef] [PubMed]
35. Garcia-Arellano, A.; Ramallal, R.; Ruiz-Canela, M.; Salas-Salvadó, J.; Corella, D.; Shivappa, N.; Schröder, H.; Hébert, J.R.; Ros, E.; Gómez-Garcia, E.; et al. Dietary Inflammatory Index and incidence of cardiovascular disease in the PREDIMED Study. Nutrients 2015, 7, 4124–4138. [CrossRef]
36. Martínez-González, M.A.; Salas-Salvadó, J.; Estruch, R.; Corella, D.; Fitó, M.; Ros, E.; PREDIMED Investigators. Benefits of the Mediterranean Diet: Insights from the PREDIMED Study. Prog. Cardiovasc. Dis. 2015, 58, 50–60.
37. Guasch-Ferré, M.; Salas-Salvadó, J.; Ros, E.; Estruch, R.; Corella, D.; Fitó, M.; Martínez-González, M.A.; PREDIMED Investigators. The PREDIMED trial, Mediterranean diet and health outcomes: How strong is the evidence? Nutr. Metab. Cardiovasc. Dis. 2017, 27, 624–632.
38. Erdrich, S.; Bishop, K.S.; Karunasinghe, N.; Han, D.Y.; Ferguson, L.R. A pilot study to investigate if New Zealand men with prostate cancer benefit from a Mediterranean-style diet. Peer J. 2015, 3, e1080. [CrossRef]
39. Gutierrez-Mariscal, F.M.; Yubero-Serrano, E.M.; Rangel-Zúñiga, O.A.; Marín, C.; García-Rios, A.; Perez-Martinez, P.; Delgado-Lista, J.; Malagón, M.M.; Tinahones, F.J.; Pérez-Jimenez, F.; et al. Postprandial activation of p53-dependent DNA repair is modified by Mediterranean diet supplemented with coenzyme Q10 in elderly subjects. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69, 886–893. [CrossRef] [PubMed]
40. Mitjavila, M.T.; Fandos, M.; Salas-Salvadó, J.; Covas, M.I.; Borrego, S.; Estruch, R.; Lamuela-Raventós, R.; Corella, D.; Martínez-Gonzalez, M.Á.; Sánchez, J.M.; et al. The Mediterranean diet improves the systemic lipid and DNA oxidative damage in metabolic syndrome individuals. A randomized, controlled, trial. Clin. Nutr. 2013, 32, 172–178. [CrossRef]
41. Gutierrez-Mariscal, F.M.; Perez-Martinez, P.; Delgado-Lista, J.; Yubero-Serrano, E.M.; Camargo, A.; Delgado-Casado, N.; Cruz-Teno, C.; Santos-Gonzalez, M.; Rodriguez-Cantalejo, F.; Castaño, J.P.; et al. Mediterranean diet supplemented with coenzyme Q10 induces postprandial changes in p53 in response to oxidative DNA damage in elderly subjects. Age 2012, 34, 389–403. [CrossRef] [PubMed]
42. Konstantinidou, V.; Covas, M.I.; Muñoz-Aguayo, D.; Khymenets, O.; de la Torre, R.; Saez, G.; del Carmen Tormos, M.; Toledo, E.; Marti, A.; Ruiz-Gutiérrez, V.; et al. In vivo nutrigenomic effects of virgin olive oil polyphenols within the frame of the Mediterranean diet: A randomized controlled trial. FASEB J. 2010, 24, 2546–2557. [CrossRef] [PubMed]
43. Urquiaga, I.; Strobel, P.; Perez, D.; Martinez, C.; Cuevas, A.; Castillo, O.; Marshall, G.; Rozowski, J.; Leighton, F. Mediterranean diet and red wine protect against oxidative damage in young volunteers. Atherosclerosis 2010, 211, 694–699. [CrossRef] [PubMed]
44. García-Calzón, S.; Martínez-González, M.A.; Razquin, C.; Arós, F.; Lapetra, J.; Martínez, J.A.; Zalba, G.; Marti, A. Mediterranean diet and telomere length in high cardiovascular risk subjects from the PREDIMED-NAVARRA study. Clin. Nutr. 2016, 35, 1399–1405. [CrossRef] [PubMed]
45. García-Calzón, S.; Martínez-González, M.A.; Razquin, C.; Corella, D.; Salas-Salvadó, J.; Martínez, J.A.; Zalba, G.; Marti, A. Pro12Ala polymorphism of the PPARγ2 gene interacts with a mediterranean diet to prevent telomere shortening in the PREDIMED-NAVARRA randomized trial. Circ. Cardiovasc. Genet. 2015, 8, 91–99. [CrossRef]
46. Müllner, E.; Brath, H.; Pleifer, S.; Schiermayr, C.; Baierl, A.; Wallner, M.; Fastian, T.; Millner, Y.; Paller, K.; Henriksen, T.; et al. Vegetables and PUFA-rich plant oil reduce DNA strand breaks in individuals with type 2 diabetes. Mol. Nutr Food Res. 2013, 57, 328–338. [CrossRef] [PubMed]
47. Zeng, L.; Wu, G.Z.; Goh, K.J.; Lee, Y.M.; Ng, C.C.; You, A.B.; Wang, J.; Jia, D.; Hao, A.; Yu, Q.; et al. Saturated fatty acids modulate cell response to DNA damage: Implication for their role in tumorigenesis. PLoS ONE 2008, 3, e2329. [CrossRef] [PubMed]
48. Bishop, K.S.; Erdrich, S.; Karunasinghe, N.; Han, D.Y.; Zhu, S.; Jesuthasan, A.; Ferguson, L.R. An investigation into the association between DNA damage and dietary fatty acid in men with prostate cancer. Nutrients 2015, 7, 405–422. [CrossRef]
49. Jenkinson, A.; Franklin, M.F.; Wahle, K.; Duthie, G.G. Dietary intakes of polyunsaturated fatty acids and indices of oxidative stress in human volunteers. Eur. J. Clin. Nutr. 1999, 53, 523–528. [CrossRef]
50. Kimura, Y.; Sato, M.; Kurotani, K.; Nanri, A.; Kawai, K.; Kasai, H.; Imaizumi, K.; Mizoue, T. PUFAs in serum cholesterol ester and oxidative DNA damage in Japanese men and women. Am. J. Clin. Nutr. 2012, 95, 1209–1214. [CrossRef]
51. Sakai, C.; Ishida, M.; Ohba, H.; Yamashita, H.; Uchida, H.; Yoshizumi, M.; Ishida, T. Fish oil omega-3 polyunsaturated fatty acids attenuate oxidative stress-induced DNA damage in vascular endothelial cells. PLoS ONE 2017, 12, e0187934. [CrossRef] [PubMed]
52. Kikugawa, K.; Yasuhara, Y.; Ando, K.; Koyama, K.; Hiramoto, K.; Suzuki, M. Protective effect of supplementation of fish oil with high n-3 polyunsaturated fatty acids against oxidative stress-induced DNA damage of rat liver in vivo. J. Agric. Food Chem. 2003, 51, 6073–6079. [CrossRef] [PubMed]
53. Dizdaroglu, M. Oxidatively induced DNA damage and its repair in cancer. Mutat. Res. Rev. Mutat. Res. 2015, 763, 212–245. [CrossRef] [PubMed]
54. Grosso, G.; Buscemi, S.; Galvano, F.; Mistretta, A.; Marventano, S.; La Vela, V.; Drago, F.; Gangi, S.; Basile, F.; Biondi, A. Mediterranean diet and cancer: Epidemiological evidence and mechanism of selected aspects. BMC Surg. 2013, 13 (Suppl. 2), S14. [CrossRef] [PubMed]
55. Schwingshackl, L.; Schwedhelm, C.; Galbete, C.; Hoffmann, G. Adherence to Mediterranean diet and risk of cancer: An updated systematic review and meta-analysis. Nutrients 2017, 9, 1063. [CrossRef] [PubMed]
56. Giacosa, A.; Barale, R.; Bavaresco, L.; Gatenby, P.; Gerbi, V.; Janssens, J.; Johnston, B.; Kas, K.; La Vecchia, C.; Mainguet, P.; et al. Cancer prevention in Europe: The Mediterranean diet as a protective choice. Eur. J. Cancer Prev. 2013, 22, 90–95. [CrossRef] [PubMed]
57. Turati, F.; Carioli, G.; Bravi, F.; Ferraroni, M.; Serraino, D.; Montella, M.; Giacosa, A.; Toffolutti, F.; Negri, E.; Levi, F.; et al. Mediterranean diet and breast cancer risk. Nutrients 2018, 10, 326. [CrossRef]
58. Grosso, G.; Biondi, A.; Galvano, F.; Mistretta, A.; Marventano, S.; Buscemi, S.; Drago, F.; Basile, F. Factors associated with colorectal cancer in the context of the Mediterranean diet: A case-control study. Nutr. Cancer 2014, 66, 558–565. [CrossRef]
59. Bravi, F.; Spei, M.E.; Polesel, J.; Di Maso, M.; Montella, M.; Ferraroni, M.; Serraino, D.; Libra, M.; Negri, E.; La Vecchia, C.; et al. Mediterranean diet and bladder cancer risk in Italy. Nutrients 2018, 10, 1061. [CrossRef]
60. Russo, G.I.; Solinas, T.; Urzì, D.; Privitera, S.; Campisi, D.; Cocci, A.; Carini, M.; Madonia, M.; Cimino, S.; Morgia, G. Adherence to Mediterranean diet and prostate cancer risk in Sicily: Population-based case-control study. Int. J. Impot. Res. 2018. [CrossRef]
61. Collins, A.R. Measuring oxidative damage to DNA and its repair with the comet assay. Biochim. Biophys. Acta 2014, 1840, 794–800. [CrossRef] [PubMed]
62. Møller, P. The comet assay: Ready for 30 more years. Mutagenesis 2018, 33, 1–7. [CrossRef] [PubMed]
63. Boccardi, V.; Esposito, A.; Rizzo, M.R.; Marfella, R.; Barbieri, M.; Paolisso, G. Mediterranean diet, telomere maintenance and health status among elderly. PLoS ONE 2013, 8, e62781. [CrossRef] [PubMed]
64. Crous-Bou, M.; Fung, T.T.; Prescott, J.; Julin, B.; Du, M.; Sun, Q.; Rexrode, K.M.; Hu, F.B.; De Vivo, I. Mediterranean diet and telomere length in nurses’ health study: Population based cohort study. BMJ 2014, 349, g6674. [CrossRef] [PubMed]
65. Gu, Y.; Honig, L.S.; Schupf, N.; Lee, J.H.; Luchsinger, J.A.; Stern, Y.; Scarmeas, N. Mediterranean diet and leukocyte telomere length in a multi-ethnic elderly population. Age 2015, 37, 24. [CrossRef] [PubMed]
66. Marin, C.; Delgado-Lista, J.; Ramirez, R.; Carracedo, J.; Caballero, J.; Perez-Martinez, P.; Gutierrez-Mariscal, F.M.; Garcia-Rios, A.; Delgado-Casado, N.; Cruz-Teno, C.; et al. Mediterranean diet reduces senescence-associated stress in endothelial cells. Age 2012, 34, 1309–1316. [CrossRef] [PubMed]
67. García-Calzón, S.; Gea, A.; Razquin, C.; Corella, D.; Lamuela-Raventós, R.M.; Martínez, J.A.; Martínez-González, M.A.; Zalba, G.; Marti, A. Longitudinal association of telomere length and obesity indices in an intervention study with a Mediterranean diet: The PREDIMED-NAVARRA trial. Int. J. Obes. 2014, 38, 177–182. [CrossRef] [PubMed]
68. García-Calzón, S.; Zalba, G.; Ruiz-Canela, M.; Shivappa, N.; Hébert, J.R.; Martínez, J.A.; Fitó, M.; Gómez-Gracia, E.; Martínez-González, M.A.; Marti, A. Dietary inflammatory index and telomere length in subjects with a high cardiovascular disease risk from the PREDIMED-NAVARRA study: Cross-sectional and longitudinal analyses over 5 y. Am. J. Clin. Nutr. 2015, 102, 897–904. [CrossRef] [PubMed]