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Journal of Diabetes •• (2014) ••–••
O R I G I N A L A RT I C L E
Meta-analysis of prospective studies on the effects of nut consumption on hypertension and type 2 diabetes mellitus Kai GUO, Zhiwen ZHOU, Yibo JIANG, Wei LI and Yigang LI Department of Cardiology, Xinhua Hospital, Shanghai Jiao Tong University, School of Medicine, Shanghai, China
Correspondence Yigang Li, Department of Cardiology, Xinhua Hospital, Shanghai Jiaotong University, School of Medicine, 1665 Kongjiang Road, Shanghai, 200092, China. Tel: +86-21-25078999-7265 Fax: +86-21-65083740 Email: [email protected] Received 4 December 2013; revised 20 April 2014; accepted 15 May 2014. doi: 10.1111/1753-0407.12173
Abstract Background: Inconclusive reports have been published on the consumption of nuts and the risk of hypertension and type 2 diabetes mellitus (T2DM). We performed a meta-analysis of prospective studies to assess the effects of nut consumption on hypertension and T2DM risks. Methods: A PUBMED and EMBASE database search was performed. Summary relative risks (SRRs) and 95% confidence intervals (CIs) were calculated using a random-effects model. Q and I2 statistics were used to examine between-study heterogeneity. Results: A total of eight articles with nine prospective cohort studies (three hypertension studies and six T2DM studies) were selected. Using random effects models, we found that compared with never/rare consumers of nuts, those consuming >2 servings per week had an 8% lower risk of hypertension (SRR = 0.92, 95% CI: 0.87–0.97, P heterogeneity = 0. 590, I2 = 0%), while consumption of nuts at one serving per week had similar risk (SRR = 0.97, 95% CI: 0.83–1.13). In addition, nuts consumption was not associated with risk of T2DM (SRRs = 0. 98, 95% CI: 0.84–1.15; Pheterogeneity = 0. 008, I2 = 67.7%) on the basis of the highest versus lowest analysis. This null association was also shown in the dose-response analysis. Conclusion: Findings from this meta-analysis indicate that consumption of nuts (>2 servings/week) may be inversely associated with hypertension risk, but not with T2DM risk. Keywords: hypertension, meta-analysis, nut consumption, type 2 diabetes mellitus.
Significant findings of the study: Nut consumption (>2 servings/week) is inversely associated with hypertension risk but not with T2DM risk. What this study adds: In addition to their health benefits, this meta-analysis revealed that the consumption of >2 servings of nuts per week offers protection against hypertension.
Introduction Hypertension, which affects one billion individuals worldwide, contributes to seven million deaths per year. Estimates predict that by 2030, the number of individuals with type 2 diabetes mellitus (T2DM) will double.1 T2DM increases the risk of cardiovascular disease, especially in women.2 Therefore, understanding the risk factors and
preventative measures of hypertension and T2DM is of paramount importance for human health. Studies in high-risk population groups have shown that weight loss, increased physical activity and consumption of fruits, vegetables, and potassium, and reduced intakes of sodium reduce the incidence of hypertension3–5 and T2DM.6,7 Therefore, with the increasing prevalence of these chronic conditions, it is not surprising that alterna-
© 2014 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
1
Nut consumption and hypertension and T2DM
K. GUO et al.
tive and complementary therapies are being explored.8 Nuts, which have been part of the human diet since pre-agricultural times, provide several nutrients and phytochemicals that may lower the risk of T2DM and hypertension. Nuts are low in saturated fats and high in mono- and polyunsaturated fatty acids (MUFAs and PUFAs, respectively) and are good sources of protein, fiber, vitamins, minerals, phytosterols, and polyphenols.9 These bioactive compounds have antioxidant and antiinflammatory properties, which increase insulin resistance and decrease the incidence of T2DM and hypertension. The evidence on the effect of nut consumption on the overall risk of T2DM and hypertension remains inconclusive.10–18 Therefore, we performed a quantitative review to summarize the available evidence of nut consumption in T2DM and hypertension following the meta-analysis of observational studies in epidemiology (MOOSE).19
Methods Search strategy For this meta-analysis, two authors (G.K and Z.Z.W.) searched PUBMED and EMBASE databases (1966 to July 2013). The search strategy included the following subject headings or keywords: (i) “nut”, “peanut”, “walnut”, “almond”, “pine”, “hazel”, “filbert”, “ginkgo”, “lotus”, or “melon seed”; and (ii) “blood pressure”, “hypertension”, “diabetes”, “T2DM”, “high glucose”, “hyperglycemia”, or “NIDDM”. We evaluated the reference lists for additional studies. Only articles written in English were included in the meta-analysis. Study selection Title, abstract, full-text articles, and study quality were evaluated by two investigators (G.K and J.Y.B.); any discrepancy was resolved by a third investigator (L.Y.G.). Studies included in the meta-analysis: (i) had a prospective cohort design assessing the effects of nut consumption on the long-term risks of hypertension and/or T2DM; and (ii) included the risk estimates and 95% confidence intervals (CIs) or standard errors for the association between nut consumption and outcomes of interest. Articles that were excluded were review articles, ecological assessments, correlation studies, and protocols; studies conducted on animals or cell lines; studies that did not report nut consumption; and studies that did not include T2DM or hypertension as the outcome of interest. Additionally, studies were excluded if they only reported cross-sectional associations.20,21 If the data were 2
duplicated in more than one study, the most recent or informative one was included in the meta-analysis.13 Data extraction Using a standardized form, two reviewers (G.K and J.Y.B.) independently extracted data from each study. The extracted data included basic information (title, authors, and publication year); study characteristics (name of the study, study design, country, and follow-up duration); participant characteristics (sample size, and number of cases with T2DM and/or hypertension); assessment methods; comparisons; risk estimates and 95% CIs; and covariates that were matched and/or adjusted for in the multivariate analysis. The reviewers extracted the risk estimates that reflected the greatest degree of control for potential confounders. Quality assessment for individual studies Two reviewers (G.K and J.Y.B.) assessed the quality of each study using the Newcastle-Ottawa quality assessment scale (NOS),22 which uses three quality parameters for cohort studies: selection, comparability, and outcome assessment. NOS assigns a maximum of four points for selection, two points for comparability, and three points for outcome. A total score of ≥7 points is indicative of high-quality studies; a total score of ≤6 points is indicative of low-quality studies. Studies that could not be evaluated by NOS because of insufficient information were considered to be low-quality studies. Statistical analyses In this study, we used a random-effects model to calculate summary relative risks (SRRs) and 95% CIs of T2DM and hypertension. This method, developed by DerSimonian and Laird, accounts for heterogeneity among studies.23 Publication bias was evaluated by Begg’s adjusted rank correlation test and funnel plot.24 Statistical significance was set at P < 0.05 (two-sided). Statistical analyses were performed with Stata Statistical Software version 11.0 (STATA, College Station, TX, USA). Q and I2 statistics were used to assess between-study heterogeneity. For Q statistics, P < 0.1 was considered to be statistically significant. I2 was the percentage of total variation across studies due to heterogeneity; I2 > 50% was indicative of significant heterogeneity and I2 < 25% was indicative of insignificant heterogeneity.25 For sensitivity analysis, we used a fixed-effects model. Additional sensitivity analyses were performed by excluding one study in the meta-analysis and calculating a pooled estimate for the remainder of the studies to evaluate whether the results were significantly affected by a single study.
© 2014 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
K. GUO et al.
Nut consumption and hypertension and T2DM
We conducted a meta-analysis of dose-response categorical data for nut consumption and risk of hypertension and T2DM. In two hypertension studies,11,12 where more than one nut consumption level fell in the categories (e.g., one serving/week and ≥2 servings/ week), we pooled the corresponding risk estimates (weighted by the inverse of their variance). In another study,10 the unit of nut consumption (g/day) was converted to the above range. For T2DM, three studies14,18 reported separate SRRs for nut consumption categories (e.g., 6). The most common selection bias was the under-representation of the study participants.
Articles identified through database searching (n = 2952): MEDLINE (n = 1171), EMBASE (n = 1781)
Duplicate articles (n = 758)
Articles after duplicates removed (n = 2194)
Articles excluded (n = 2138): title and abstract not relevant, review, mechanism studies, and comment, etc.
Hand searching (n = 6)
Full-text articles screened (n = 56)
Articles excluded (n = 54): Did not evaluate the association for T2DM/HBP (n = 41) Did not report measures of variability (n = 6) Presented on dietary patterns and T2DM/HBP (n = 5) Cross-sectional studies (n = 2)
Articles included in meta-analysis (n = 8)
Figure 1 Flow diagram of systematic literature search on nut intake and risk of hypertension and type 2 diabetes mellitus (T2DM).
3 Articles on HBP
5 Articles (6 studies) on T2DM
© 2014 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
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Nut consumption and hypertension and T2DM Table 1
K. GUO et al.
Characteristics of the studies of the association between nut consumption and hypertension
Author/ Publication year/Country Hypertension Steffen/ 2005/ Norway10
Study characteristics
CARDIA: Populationbased,prospective cohort of 4304 M + F; age:18–30
Cases, n
591
Follow-up, years
Dietary assessment
15
Exposure details
Validated FFQ
SBP ≥ 130 mm Hg, DBP ≥ 85 mm Hg, or the use of antihypertensive medications
Nuts: 0.3 times/day
1.0 0.84 (0.73–0.98) 0.85 (0.72–0.99)
Nuts: 0 servings/week 1–3 servings/month 1 servings/week 2–6 servings/week ≥7 servings/week Nuts: 0 servings/week 1–3 servings/month 1 serving/week ≥2 servings/week
1.0 0.97 (0.91–1.03) 0.98 (0.92–1.05) 0.96 (0.89–1.03) 0.82 (0.71–0.94)
Nuts 0 times/week 2 servings/week to ≥7 servings/ week, although the lowest levels were relatively uniform. In addition, sensitivity analyses revealed that significant heterogeneity emerged from the IWHS cohort;14 when this study was removed, the model became much more homogeneous. Finally, because we did not attempt to uncover unpublished studies or include studies with insufficient information to estimate a summary risk estimate, the possibility of publication bias is inevitable even though no significant evidence of publication bias was observed. In summary, findings from this meta-analysis suggested an inverse association between nut consumption (> 2 servings/week) and hypertension risk. However, nut consumption was found not to be associated with T2DM risk. Although it is too premature to suggest the consumption of nuts for the prevention of T2DM, moderate intake of nuts as part of a healthy diet can reduce the risk factors of diabetes, including elevated serum lipids, inflammation, and obesity.42,48 Therefore, a moderate consumption of nuts might prevent hypertension and T2DM in healthy subjects. Further studies with prospective designs that use validated questionnaires and control for important confounders are warranted.
Acknowledgement No funding received.
Disclosure None declared.
Nut consumption and hypertension and T2DM
References 1. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010; 87: 4–14. 2. Pan WH, Cedres LB, Liu K et al. Relationship of clinical diabetes and asymptomatic hyperglycemia to risk of coronary heart disease mortality in men and women. Am J Epidemiol. 1986; 123: 504–16. 3. Stolarz-Skrzypek K, Bednarski A, Czarnecka D, Kawecka-Jaszcz K, Staessen JA. Sodium and potassium and the pathogenesis of hypertension. Curr Hypertens Rep. 2013; 15: 122–30. 4. Molmen-Hansen HE, Stolen T, Tjonna AE et al. Aerobic interval training reduces blood pressure and improves myocardial function in hypertensive patients. Eur J Prev Cardiol. 2012; 19: 151–60. 5. Tsioufis C, Kasiakogias A, Tsiachris D et al. Metabolic syndrome and exaggerated blood pressure response to exercise in newly diagnosed hypertensive patients. Eur J Prev Cardiol. 2012; 19: 467–73. 6. Tuomilehto J, Lindstrom J, Eriksson JG et al. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med. 2001; 344: 1343–50. 7. Knowler WC, Barrett-Connor E, Fowler SE et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med. 2002; 346: 393– 403. 8. Rahman K, Lowe GM. Garlic and cardiovascular disease: A critical review. J Nutr. 2006; 136: 736S– 40S. 9. Phillips KM, Ruggio DM, Ashraf-Khorassani M. Phytosterol composition of nuts and seeds commonly consumed in the United States. J Agric Food Chem. 2005; 53: 9436–45. 10. Steffen LM, Kroenke CH, Yu X et al. Associations of plant food, dairy product, and meat intakes with 15-y incidence of elevated blood pressure in young black and white adults: The Coronary Artery Risk Development in Young Adults (CARDIA) Study. Am J Clin Nutr. 2005; 82: 1169–77. 11. Djousse L, Rudich T, Gaziano JM. Nut consumption and risk of hypertension in US male physicians. Clin Nutr. 2009; 28: 10–4. 12. Martinez-Lapiscina EH, Pimenta AM, Beunza JJ, Bes-Rastrollo M, Martinez JA, Martinez-Gonzalez MA. Nut consumption and incidence of hypertension: The SUN prospective cohort. Nutr Metab Cardiovasc Dis. 2010; 20: 359–65. 13. Jiang R, Manson JE, Stampfer MJ, Liu S, Willett WC, Hu FB. Nut and peanut butter consumption and risk of type 2 diabetes in women. JAMA. 2002; 288: 2554–60. 14. Parker ED, Harnack LJ, Folsom AR. Nut consumption and risk of type 2 diabetes. JAMA. 2003; 290: 38–9; author reply 39–40. 15. Montonen J, Jarvinen R, Heliovaara M, Reunanen A, Aromaa A, Knekt P. Food consumption and the incidence of type II diabetes mellitus. Eur J Clin Nutr. 2005; 59: 441–8.
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16. Villegas R, Gao YT, Yang G et al. Legume and soy food intake and the incidence of type 2 diabetes in the Shanghai Women’s Health Study. Am J Clin Nutr. 2008; 87: 162–7. 17. Kochar J, Gaziano JM, Djousse L. Nut consumption and risk of type II diabetes in the Physicians’ Health Study. Eur J Clin Nutr. 2010; 64: 75–9. 18. Pan A, Sun Q, Manson JE, Willett WC, Hu FB. Walnut consumption is associated with lower risk of type 2 diabetes in women. J Nutr. 2013; 143: 512–18. 19. Stroup DF, Berlin JA, Morton SC et al. Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000; 283: 2008– 12. 20. Alvarez Leon E, Henriquez P, Serra-Majem L. Mediterranean diet and metabolic syndrome: A cross-sectional study in the Canary Islands. Public Health Nutr. 2006; 9: 1089–98. 21. Ibarrola-Jurado N, Bullo M, Guasch-Ferre M et al. Cross-sectional assessment of nut consumption and obesity, metabolic syndrome and other cardiometabolic risk factors: The PREDIMED study. PLoS ONE. 2013; 8: e57367. 22. Wells GA, Shea B, O’Connell D et al. The NewcastleOttawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available from: http:// www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed 15 June 2012). 23. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7: 177–88. 24. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994; 50: 1088–101. 25. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003; 327: 557–60. 26. Estruch R, Martinez-Gonzalez MA, Corella D et al. Effects of a Mediterranean-style diet on cardiovascular risk factors: A randomized trial. Ann Intern Med. 2006; 145: 1–11. 27. Virtanen JK, Nyantika AN, Kauhanen J, Voutilainen S, Tuomainen TP. Serum long-chain n-3 polyunsaturated fatty acids, methylmercury and blood pressure in an older population. Hypertens Res. 2012; 35: 1000–4. 28. Cabo J, Alonso R, Mata P. Omega-3 fatty acids and blood pressure. Br J Nutr. 2012; 107 (Suppl. 2): S195– 200. 29. Gebauer SK, Psota TL, Harris WS, Kris-Etherton PM. n-3 fatty acid dietary recommendations and food sources to achieve essentiality and cardiovascular benefits. Am J Clin Nutr. 2006; 83: 1526S–35S. 30. Kris-Etherton PM, Zhao G, Binkoski AE, Coval SM, Etherton TD. The effects of nuts on coronary heart disease risk. Nutr Rev. 2001; 59: 103–11. 31. Kass L, Weekes J, Carpenter L. Effect of magnesium supplementation on blood pressure: A meta-analysis. Eur J Clin Nutr. 2012; 66: 411–18. 32. Streppel MT, Arends LR, van ’t Veer P, Grobbee DE, Geleijnse JM. Dietary fiber and blood pressure: A meta10
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analysis of randomized placebo-controlled trials. Arch Intern Med. 2005; 165: 150–6. Lei J, Vodovotz Y, Tzeng E, Billiar TR. Nitric oxide, a protective molecule in the cardiovascular system. Nitric Oxide. 2013; 35: 175–85. Vasdev S, Stuckless J. Antihypertensive effects of dietary protein and its mechanism. Int J Angiol. 2010; 19: e7–e 20. Ye EQ, Chacko SA, Chou EL, Kugizaki M, Liu S. Greater whole-grain intake is associated with lower risk of type 2 diabetes, cardiovascular disease, and weight gain. J Nutr. 2012; 142: 1304–13. Hruby A, Meigs JB, O’Donnell CJ, Jacques PF, McKeown NM. Higher magnesium intake reduces risk of impaired glucose and insulin metabolism and progression from prediabetes to diabetes in middle-aged americans. Diabetes Care. 2014; 37: 419–27. Liu HQ, Qiu Y, Mu Y et al. A high ratio of dietary n-3/n-6 polyunsaturated fatty acids improves obesitylinked inflammation and insulin resistance through suppressing activation of TLR4 in SD rats. Nutr Res. 2013; 33: 849–58. Salvini S, Hunter DJ, Sampson L et al. Food-based validation of a dietary questionnaire: The effects of week-toweek variation in food consumption. Int J Epidemiol. 1989; 18: 858–67. Colditz GA, Martin P, Stampfer MJ et al. Validation of questionnaire information on risk factors and disease outcomes in a prospective cohort study of women. Am J Epidemiol. 1986; 123: 894–900. Qin X, Jackson R, Marshall R et al. Modelling the potential impact of population-wide and targeted high-risk blood pressure-lowering strategies on cardiovascular disease in China. Eur J Cardiovasc Prev Rehabil. 2009; 16: 96–101. Sanchez-Villegas A, Bes-Rastrollo M, MartinezGonzalez MA, Serra-Majem L. Adherence to a Mediterranean dietary pattern and weight gain in a follow-up study: The SUN cohort. Int J Obes (Lond). 2006; 30: 350–8. Bes-Rastrollo M, Wedick NM, Martinez-Gonzalez MA, Li TY, Sampson L, Hu FB. Prospective study of nut consumption, long-term weight change, and obesity risk in women. Am J Clin Nutr. 2009; 89: 1913–19. Torabian S, Haddad E, Rajaram S, Banta J, Sabate J. Acute effect of nut consumption on plasma total polyphenols, antioxidant capacity and lipid peroxidation. J Hum Nutr Diet. 2009; 22: 64–71. Cohen AE, Johnston CS. Almond ingestion at mealtime reduces postprandial glycemia and chronic ingestion reduces hemoglobin A(1c) in individuals with wellcontrolled type 2 diabetes mellitus. Metabolism. 2011; 60: 1312–17. Li SC, Liu YH, Liu JF, Chang WH, Chen CM, Chen CY. Almond consumption improved glycemic control and lipid profiles in patients with type 2 diabetes mellitus. Metabolism. 2011; 60: 474–9. Lovejoy JC, Most MM, Lefevre M, Greenway FL, Rood JC. Effect of diets enriched in almonds on insulin action and serum lipids in adults with normal glucose
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tolerance or type 2 diabetes. Am J Clin Nutr. 2002; 76: 1000–6. 47. Altorf-van der Kuil W, Engberink MF, van Rooij FJ et al. Dietary protein and risk of hypertension in a Dutch older population: The Rotterdam study. J Hypertens. 2010; 28: 2394–400.
Nut consumption and hypertension and T2DM
48. Banel DK, Hu FB. Effects of walnut consumption on blood lipids and other cardiovascular risk factors: A meta-analysis and systematic review. Am J Clin Nutr. 2009; 90: 56–63.
© 2014 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
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Journal of Diabetes •• (2014) ••–••
O R I G I N A L A RT I C L E
Meta-analysis of prospective studies on the effects of nut consumption on hypertension and type 2 diabetes mellitus Kai GUO, Zhiwen ZHOU, Yibo JIANG, Wei LI and Yigang LI Department of Cardiology, Xinhua Hospital, Shanghai Jiao Tong University, School of Medicine, Shanghai, China
Correspondence Yigang Li, Department of Cardiology, Xinhua Hospital, Shanghai Jiaotong University, School of Medicine, 1665 Kongjiang Road, Shanghai, 200092, China. Tel: +86-21-25078999-7265 Fax: +86-21-65083740 Email: [email protected] Received 4 December 2013; revised 20 April 2014; accepted 15 May 2014. doi: 10.1111/1753-0407.12173
Abstract Background: Inconclusive reports have been published on the consumption of nuts and the risk of hypertension and type 2 diabetes mellitus (T2DM). We performed a meta-analysis of prospective studies to assess the effects of nut consumption on hypertension and T2DM risks. Methods: A PUBMED and EMBASE database search was performed. Summary relative risks (SRRs) and 95% confidence intervals (CIs) were calculated using a random-effects model. Q and I2 statistics were used to examine between-study heterogeneity. Results: A total of eight articles with nine prospective cohort studies (three hypertension studies and six T2DM studies) were selected. Using random effects models, we found that compared with never/rare consumers of nuts, those consuming >2 servings per week had an 8% lower risk of hypertension (SRR = 0.92, 95% CI: 0.87–0.97, P heterogeneity = 0. 590, I2 = 0%), while consumption of nuts at one serving per week had similar risk (SRR = 0.97, 95% CI: 0.83–1.13). In addition, nuts consumption was not associated with risk of T2DM (SRRs = 0. 98, 95% CI: 0.84–1.15; Pheterogeneity = 0. 008, I2 = 67.7%) on the basis of the highest versus lowest analysis. This null association was also shown in the dose-response analysis. Conclusion: Findings from this meta-analysis indicate that consumption of nuts (>2 servings/week) may be inversely associated with hypertension risk, but not with T2DM risk. Keywords: hypertension, meta-analysis, nut consumption, type 2 diabetes mellitus.
Significant findings of the study: Nut consumption (>2 servings/week) is inversely associated with hypertension risk but not with T2DM risk. What this study adds: In addition to their health benefits, this meta-analysis revealed that the consumption of >2 servings of nuts per week offers protection against hypertension.
Introduction Hypertension, which affects one billion individuals worldwide, contributes to seven million deaths per year. Estimates predict that by 2030, the number of individuals with type 2 diabetes mellitus (T2DM) will double.1 T2DM increases the risk of cardiovascular disease, especially in women.2 Therefore, understanding the risk factors and
preventative measures of hypertension and T2DM is of paramount importance for human health. Studies in high-risk population groups have shown that weight loss, increased physical activity and consumption of fruits, vegetables, and potassium, and reduced intakes of sodium reduce the incidence of hypertension3–5 and T2DM.6,7 Therefore, with the increasing prevalence of these chronic conditions, it is not surprising that alterna-
© 2014 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
1
Nut consumption and hypertension and T2DM
K. GUO et al.
tive and complementary therapies are being explored.8 Nuts, which have been part of the human diet since pre-agricultural times, provide several nutrients and phytochemicals that may lower the risk of T2DM and hypertension. Nuts are low in saturated fats and high in mono- and polyunsaturated fatty acids (MUFAs and PUFAs, respectively) and are good sources of protein, fiber, vitamins, minerals, phytosterols, and polyphenols.9 These bioactive compounds have antioxidant and antiinflammatory properties, which increase insulin resistance and decrease the incidence of T2DM and hypertension. The evidence on the effect of nut consumption on the overall risk of T2DM and hypertension remains inconclusive.10–18 Therefore, we performed a quantitative review to summarize the available evidence of nut consumption in T2DM and hypertension following the meta-analysis of observational studies in epidemiology (MOOSE).19
Methods Search strategy For this meta-analysis, two authors (G.K and Z.Z.W.) searched PUBMED and EMBASE databases (1966 to July 2013). The search strategy included the following subject headings or keywords: (i) “nut”, “peanut”, “walnut”, “almond”, “pine”, “hazel”, “filbert”, “ginkgo”, “lotus”, or “melon seed”; and (ii) “blood pressure”, “hypertension”, “diabetes”, “T2DM”, “high glucose”, “hyperglycemia”, or “NIDDM”. We evaluated the reference lists for additional studies. Only articles written in English were included in the meta-analysis. Study selection Title, abstract, full-text articles, and study quality were evaluated by two investigators (G.K and J.Y.B.); any discrepancy was resolved by a third investigator (L.Y.G.). Studies included in the meta-analysis: (i) had a prospective cohort design assessing the effects of nut consumption on the long-term risks of hypertension and/or T2DM; and (ii) included the risk estimates and 95% confidence intervals (CIs) or standard errors for the association between nut consumption and outcomes of interest. Articles that were excluded were review articles, ecological assessments, correlation studies, and protocols; studies conducted on animals or cell lines; studies that did not report nut consumption; and studies that did not include T2DM or hypertension as the outcome of interest. Additionally, studies were excluded if they only reported cross-sectional associations.20,21 If the data were 2
duplicated in more than one study, the most recent or informative one was included in the meta-analysis.13 Data extraction Using a standardized form, two reviewers (G.K and J.Y.B.) independently extracted data from each study. The extracted data included basic information (title, authors, and publication year); study characteristics (name of the study, study design, country, and follow-up duration); participant characteristics (sample size, and number of cases with T2DM and/or hypertension); assessment methods; comparisons; risk estimates and 95% CIs; and covariates that were matched and/or adjusted for in the multivariate analysis. The reviewers extracted the risk estimates that reflected the greatest degree of control for potential confounders. Quality assessment for individual studies Two reviewers (G.K and J.Y.B.) assessed the quality of each study using the Newcastle-Ottawa quality assessment scale (NOS),22 which uses three quality parameters for cohort studies: selection, comparability, and outcome assessment. NOS assigns a maximum of four points for selection, two points for comparability, and three points for outcome. A total score of ≥7 points is indicative of high-quality studies; a total score of ≤6 points is indicative of low-quality studies. Studies that could not be evaluated by NOS because of insufficient information were considered to be low-quality studies. Statistical analyses In this study, we used a random-effects model to calculate summary relative risks (SRRs) and 95% CIs of T2DM and hypertension. This method, developed by DerSimonian and Laird, accounts for heterogeneity among studies.23 Publication bias was evaluated by Begg’s adjusted rank correlation test and funnel plot.24 Statistical significance was set at P < 0.05 (two-sided). Statistical analyses were performed with Stata Statistical Software version 11.0 (STATA, College Station, TX, USA). Q and I2 statistics were used to assess between-study heterogeneity. For Q statistics, P < 0.1 was considered to be statistically significant. I2 was the percentage of total variation across studies due to heterogeneity; I2 > 50% was indicative of significant heterogeneity and I2 < 25% was indicative of insignificant heterogeneity.25 For sensitivity analysis, we used a fixed-effects model. Additional sensitivity analyses were performed by excluding one study in the meta-analysis and calculating a pooled estimate for the remainder of the studies to evaluate whether the results were significantly affected by a single study.
© 2014 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
K. GUO et al.
Nut consumption and hypertension and T2DM
We conducted a meta-analysis of dose-response categorical data for nut consumption and risk of hypertension and T2DM. In two hypertension studies,11,12 where more than one nut consumption level fell in the categories (e.g., one serving/week and ≥2 servings/ week), we pooled the corresponding risk estimates (weighted by the inverse of their variance). In another study,10 the unit of nut consumption (g/day) was converted to the above range. For T2DM, three studies14,18 reported separate SRRs for nut consumption categories (e.g., 6). The most common selection bias was the under-representation of the study participants.
Articles identified through database searching (n = 2952): MEDLINE (n = 1171), EMBASE (n = 1781)
Duplicate articles (n = 758)
Articles after duplicates removed (n = 2194)
Articles excluded (n = 2138): title and abstract not relevant, review, mechanism studies, and comment, etc.
Hand searching (n = 6)
Full-text articles screened (n = 56)
Articles excluded (n = 54): Did not evaluate the association for T2DM/HBP (n = 41) Did not report measures of variability (n = 6) Presented on dietary patterns and T2DM/HBP (n = 5) Cross-sectional studies (n = 2)
Articles included in meta-analysis (n = 8)
Figure 1 Flow diagram of systematic literature search on nut intake and risk of hypertension and type 2 diabetes mellitus (T2DM).
3 Articles on HBP
5 Articles (6 studies) on T2DM
© 2014 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
3
Nut consumption and hypertension and T2DM Table 1
K. GUO et al.
Characteristics of the studies of the association between nut consumption and hypertension
Author/ Publication year/Country Hypertension Steffen/ 2005/ Norway10
Study characteristics
CARDIA: Populationbased,prospective cohort of 4304 M + F; age:18–30
Cases, n
591
Follow-up, years
Dietary assessment
15
Exposure details
Validated FFQ
SBP ≥ 130 mm Hg, DBP ≥ 85 mm Hg, or the use of antihypertensive medications
Nuts: 0.3 times/day
1.0 0.84 (0.73–0.98) 0.85 (0.72–0.99)
Nuts: 0 servings/week 1–3 servings/month 1 servings/week 2–6 servings/week ≥7 servings/week Nuts: 0 servings/week 1–3 servings/month 1 serving/week ≥2 servings/week
1.0 0.97 (0.91–1.03) 0.98 (0.92–1.05) 0.96 (0.89–1.03) 0.82 (0.71–0.94)
Nuts 0 times/week 2 servings/week to ≥7 servings/ week, although the lowest levels were relatively uniform. In addition, sensitivity analyses revealed that significant heterogeneity emerged from the IWHS cohort;14 when this study was removed, the model became much more homogeneous. Finally, because we did not attempt to uncover unpublished studies or include studies with insufficient information to estimate a summary risk estimate, the possibility of publication bias is inevitable even though no significant evidence of publication bias was observed. In summary, findings from this meta-analysis suggested an inverse association between nut consumption (> 2 servings/week) and hypertension risk. However, nut consumption was found not to be associated with T2DM risk. Although it is too premature to suggest the consumption of nuts for the prevention of T2DM, moderate intake of nuts as part of a healthy diet can reduce the risk factors of diabetes, including elevated serum lipids, inflammation, and obesity.42,48 Therefore, a moderate consumption of nuts might prevent hypertension and T2DM in healthy subjects. Further studies with prospective designs that use validated questionnaires and control for important confounders are warranted.
Acknowledgement No funding received.
Disclosure None declared.
Nut consumption and hypertension and T2DM
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