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Vegetable diversity in relation with subclinical atherosclerosis and 15-year atherosclerotic vascular disease deaths in older adult women

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Abstract

Purpose

Increasing vegetable intake and diversity are recommended to maintain better health. Evidence for the health benefits of vegetable diversity, separate from total intake, is scarce. We aimed to investigate the associations of vegetable diversity with subclinical measures of atherosclerosis and atherosclerotic vascular disease (ASVD) mortality.

Methods

Vegetable diversity was assessed within a validated food frequency questionnaire using a single question, ‘How many different vegetables do you usually consume each day (< 1 to ≥ 6 per day)’. Cox proportional hazards modelling was used to examine the association between vegetable diversity and ASVD mortality in 1226 women aged ≥ 70 years without clinical ASVD or diabetes mellitus at baseline (1998). In 2001, B-mode ultrasonography was used to measure common carotid artery intima–media thickness (CCA-IMT) (n = 954) and carotid plaque severity (n = 968).

Results

Over 15 years (15,947 person-years) of follow-up, 238 ASVD-related deaths were recorded. For each additional different vegetable consumed per day, there was 17% lower hazard for ASVD mortality (HR = 0.83, 95% CI 0.78, 0.93, P = 0.001); a 1.7% lower mean CCA-IMT (B ± SE: − 0.013 ± 0.004, P < 0.001); and a 1.8% lower maximum CCA-IMT (B ± SE: − 0.017 ± 0.004, P < 0.001). Further adjustment for total vegetable intake attenuated the association between vegetable diversity and ASVD mortality (P = 0.114), but not CCA-IMT (P = 0.024). No association was observed between vegetable diversity and carotid plaque severity (P > 0.05).

Conclusions

Vegetable diversity may contribute to benefits in lowering risk of ASVD in older women. The reduction in risk is partly explained by increased total vegetable consumption.

Clinical trial registry

The Perth Longitudinal Study of Aging in Women (PLSAW) trial registration ID is ACTRN12617000640303. This study was retrospectively registered on the Australian New Zealand Clinical Trials Registry at http://www.anzctr.org.au.

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Abbreviations

ASVD:

Atherosclerotic vascular disease

CCA-IMT:

Common carotid artery intima–media thickness

CKD-EPI:

Chronic Kidney Disease Epidemiology Collaboration

eGFR:

Estimated glomerular filtration rate

FRS:

Framingham risk scores

HDL:

High-density lipoprotein

ICD:

International Classification of Diseases

ICPC-Plus:

International Classification of Primary Care-Plus

LDL:

Low-density lipoprotein

NRVs:

Nutrient reference values

PLSAW:

Perth Longitudinal Study of Aging in Women

WADLS:

Western Australian Data Linkage System (WADLS).

References

  1. GBD 2013 Mortality and Causes of Death Collaborators (2015) Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 385(9963):117–171

    Article  Google Scholar 

  2. Gan Y, Tong X, Li L, Cao S, Yin X, Gao C, Herath C, Li W, Jin Z, Chen Y, Lu Z (2015) Consumption of fruit and vegetable and risk of coronary heart disease: a meta-analysis of prospective cohort studies. Int J Cardiol 183:129–137. https://doi.org/10.1016/j.ijcard.2015.01.077

    Article  PubMed  Google Scholar 

  3. Aune D, Giovannucci E, Boffetta P, Fadnes LT, Keum N, Norat T, Greenwood DC, Riboli E, Vatten LJ, Tonstad S (2017) Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality: a systematic review and dose-response meta-analysis of prospective studies. Int J Epidemiol 46(3):1029–1056

    Article  Google Scholar 

  4. Hu D, Huang J, Wang Y, Zhang D, Qu Y (2014) Fruits and vegetables consumption and risk of stroke: a meta-analysis of prospective cohort studies. Stroke 45(6):1613–1619. https://doi.org/10.1161/strokeaha.114.004836

    Article  CAS  PubMed  Google Scholar 

  5. Wang X, Ouyang Y, Liu J, Zhu M, Zhao G, Bao W, Hu FB (2014) Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: systematic review and dose-response meta-analysis of prospective cohort studies. BMJ 349:1–14. https://doi.org/10.1136/bmj.g4490

    Article  CAS  Google Scholar 

  6. Liu RH (2013) Health-promoting components of fruits and vegetables in the diet. Adv Nutr 4:384S–392S

    Article  CAS  Google Scholar 

  7. Threapleton DE, Greenwood DC, Evans CEL, Cleghorn CL, Nykjaer C, Woodhead C, Cade JE, Gale CP, Burley VJ (2013) Dietary fibre intake and risk of cardiovascular disease: systematic review and meta-analysis. Br Med J 347. https://doi.org/10.1136/bmj.f6879

    Article  Google Scholar 

  8. Del Gobbo LC, Imamura F, Wu JHY, de Oliveira Otto MC, Chiuve SE, Mozaffarian D (2013) Circulating and dietary magnesium and risk of cardiovascular disease: a systematic review and meta-analysis of prospective studies. Am J Clin Nutr 98(1):160–173. https://doi.org/10.3945/ajcn.112.053132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Aburto NJ, Hanson S, Gutierrez H, Hooper L, Elliott P, Cappuccio FP (2013) Effect of increased potassium intake on cardiovascular risk factors and disease: systematic review and meta-analyses. Br Med J 346:f1378. https://doi.org/10.1136/bmj.f1378

    Article  Google Scholar 

  10. Kim Y, Je Y (2017) Flavonoid intake and mortality from cardiovascular disease and all causes: a meta-analysis of prospective cohort studies. Clin Nutr ESPEN 20(Suppl C):68–77

    Article  Google Scholar 

  11. Shea MK, Booth SL, Weiner DE, Brinkley TE, Kanaya AM, Murphy RA, Simonsick EM, Wassel CL, Vermeer C, Kritchevsky SB (2017) Circulating vitamin K is inversely associated with incident cardiovascular disease risk among those treated for hypertension in the Health, Aging, and Body Composition Study (Health ABC). J Nutr 147(5):888–895

    Article  CAS  Google Scholar 

  12. Moser M, Chun O (2016) Vitamin C and heart health: a review based on findings from epidemiologic studies. Int J Mol Sci 17(8):1328

    Article  Google Scholar 

  13. Blekkenhorst LC, Bondonno CP, Lewis JR, Devine A, Woodman RJ, Croft KD, Lim WH, Wong G, Beilin LJ, Prince RL, Hodgson JM (2017) Association of dietary nitrate with atherosclerotic vascular disease mortality: a prospective cohort study of older adult women. Am J Clin Nutr 106(1):207–216

    Article  Google Scholar 

  14. Bondonno CP, Blekkenhorst LC, Prince RL, Ivey KL, Lewis JR, Devine A, Woodman RJ, Lundberg JO, Croft KD, Thompson PL, Hodgson JM (2017) Association of vegetable nitrate intake with carotid atherosclerosis and ischemic cerebrovascular disease in older women. Stroke 48(8):1–6

    Google Scholar 

  15. Vazquez-Prieto MA, Miatello RM (2010) Organosulfur compounds and cardiovascular disease. Mol Aspects Med 31(6):540–545

    Article  CAS  Google Scholar 

  16. Azadbakht L, Mirmiran P, Esmaillzadeh A, Azizi F (2006) Dietary diversity score and cardiovascular risk factors in Tehranian adults. Public Health Nutr 9(6):728–736

    Article  Google Scholar 

  17. Kant AK, Schatzkin A, Harris TB, Ziegler RG, Block G (1993) Dietary diversity and subsequent mortality in the First National Health and Nutrition Examination Survey Epidemiologic Follow-up Study. Am J Clin Nutr 57(3):434–440

    Article  CAS  Google Scholar 

  18. Fernandez E, D’Avanzo B, Negri E, Franceschi S, La Vecchia C (1996) Diet diversity and the risk of colorectal cancer in northern Italy. Cancer Epidemiol Biomarkers Prev 5(6):433–436

    CAS  PubMed  Google Scholar 

  19. de Oliveira Otto MC, Padhye NS, Bertoni AG, Jacobs DR Jr, Mozaffarian D (2015) Everything in moderation - dietary diversity and quality, central obesity and risk of diabetes. PLoS One 10(10):e0141341. https://doi.org/10.1371/journal.pone.0141341

    Article  CAS  PubMed Central  Google Scholar 

  20. Jansen MCJF, Bueno-de-Mesquita HB, Feskens EJM, Streppel MT, Kok FJ, Kromhout D (2004) Reports: quantity and variety of fruit and vegetable consumption and cancer risk. Nutr Cancer 48(2):142–148

    Article  Google Scholar 

  21. Almeida-de-Souza J, Santos R, Lopes L, Abreu S, Moreira C, Padrão P, Mota J, Moreira P (2017) Associations between fruit and vegetable variety and low-grade inflammation in Portuguese adolescents from LabMed Physical Activity Study. Eur J Nutr. https://doi.org/10.1007/s00394-017-1479-y

    Article  PubMed  Google Scholar 

  22. Bhupathiraju SN, Tucker KL (2011) Greater variety in fruit and vegetable intake is associated with lower inflammation in Puerto Rican adults. Am J Clin Nutr 93(1):37–46

    Article  CAS  Google Scholar 

  23. Cooper AJ, Sharp SJ, Lentjes MAH, Luben RN, Khaw K-T, Wareham NJ, Forouhi NG (2012) A prospective study of the association between quantity and variety of fruit and vegetable intake and incident type 2 diabetes. Diabetes Care 35(6):1293–1300

    Article  Google Scholar 

  24. Blekkenhorst LC, Bondonno CP, Lewis JR, Devine A, Zhu K, Lim WH, Woodman RJ, Beilin LJ, Prince RL, Hodgson JM (2017) Cruciferous and allium vegetable intakes are inversely associated with 15-year atherosclerotic vascular disease deaths in older adult women. J Am Heart Assoc 6(10):1–15

    Article  Google Scholar 

  25. Britt H, Scahill S, Miller G (1997) ICPC PLUS for community health? A feasibility study. Health Inf Manag 27(4):171–175

    CAS  PubMed  Google Scholar 

  26. World Health Organization (1977) Manual of the International Statistical Classification of Diseases, Injuries and Causes of Death, 9th Revision (ICD-9). World Health Organization, Geneva

    Google Scholar 

  27. National Centre for Classification in Health (1998) International Statistical Classification of Diseases and Related Health Problems, 10th Revision, Australian Modification (ICD-10-AM). National Centre for Classification in Health, Sydney

    Google Scholar 

  28. Salonen JT, Salonen R (1993) Ultrasound B-mode imaging in observational studies of atherosclerotic progression. Circulation 87(3 Suppl):II56–I65

    CAS  PubMed  Google Scholar 

  29. Lewis JR, Zhu K, Thompson PL, Prince RL (2014) The effects of 3 years of calcium supplementation on common carotid artery intimal medial thickness and carotid atherosclerosis in older women: an ancillary study of the CAIFOS randomized controlled trial. J Bone Miner Res 29(3):534–541. https://doi.org/10.1002/jbmr.2117

    Article  CAS  PubMed  Google Scholar 

  30. Wilson PWF, Hoeg JM, D’Agostino RB, Silbershatz H, Belanger AM, Poehlmann H, O’Leary D, Wolf PA (1997) Cumulative effects of high cholesterol levels, high blood pressure, and cigarette smoking on carotid stenosis. N Engl J Med 337(8):516–522. https://doi.org/10.1056/nejm199708213370802

    Article  CAS  PubMed  Google Scholar 

  31. Ireland P, Jolley D, Giles G, O’Dea K, Powles J, Rutishauser I, Wahlqvist ML, Williams J (1994) Development of the Melbourne FFQ: a food frequency questionnaire for use in an Australian prospective study involving an ethnically diverse cohort. Asia Pac J Clin Nutr 3(1):19–31

    CAS  PubMed  Google Scholar 

  32. Hodge A, Patterson AJ, Brown WJ, Ireland P, Giles G (2000) The Anti Cancer Council of Victoria FFQ: relative validity of nutrient intakes compared with weighed food records in young to middle-aged women in a study of iron supplementation. Aust N Z J Public Health 24(6):576–583

    Article  CAS  Google Scholar 

  33. Australian Bureau of Statistics (2015) National Health Survey: first results, 2014–15. Commonwealth of Australia

  34. Lewis J, Milligan G, Hunt A (1995) NUTTAB95 Nutrient Data Table for Use in Australia. Australian Government Publishing Service, Canberra

    Google Scholar 

  35. Fulgoni VL, Keast DR, Drewnowski A (2009) Development and validation of the nutrient-rich foods index: a tool to measure nutritional quality of foods. J Nutr 139(8):1549–1554

    Article  Google Scholar 

  36. National Health and Medical Research Council (2006) Nutrient reference values for Australia and New Zealand. Canberra

  37. Australian Bureau of Statistics (1998) Socio-economic indexes for areas. Catalogue Number 2039.0. ABS, Canberra

    Google Scholar 

  38. Lewis JR, Schousboe JT, Lim WH, Wong G, Wilson KE, Zhu K, Thompson PL, Kiel DP, Prince RL (2018) Long-term atherosclerotic vascular disease risk and prognosis in elderly women with abdominal aortic calcification on lateral spine images captured during bone density testing: a prospective study. J Bone Miner Res 33(6):1001–1010. https://doi.org/10.1002/jbmr.3405

    Article  PubMed  PubMed Central  Google Scholar 

  39. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612

    Article  Google Scholar 

  40. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clin Chem 18(6):499–502

    Article  CAS  Google Scholar 

  41. D’Agostino RB, Vasan RS, Pencina MJ, Wolf PA, Cobain M, Massaro JM, Kannel WB (2008) General cardiovascular risk profile for use in primary care: the Framingham Heart Study. Circ J 117(6):743–753. https://doi.org/10.1161/circulationaha.107.699579

    Article  Google Scholar 

  42. Hodgson JM, Prince RL, Woodman RJ, Bondonno CP, Ivey KL, Bondonno N, Rimm EB, Ward NC, Croft KD, Lewis JR (2016) Apple intake is inversely associated with all-cause and disease-specific mortality in elderly women. Br J Nutr 115(5):860–867

    Article  CAS  Google Scholar 

  43. Lupoli R, Vaccaro A, Ambrosino P, Poggio P, Amato M, Di Minno MND (2017) Impact of vitamin D deficiency on subclinical carotid atherosclerosis: a pooled analysis of cohort studies. J Clin Endocrinol Metab 102(7):2146–2153

    Article  Google Scholar 

  44. Kant AK, Schatzkin A, Ziegler RG (1995) Dietary diversity and subsequent cause-specific mortality in the NHANES I epidemiologic follow-up study. J Am Coll Nutr 14(3):233–238

    Article  CAS  Google Scholar 

  45. Azadbakht L, Mirmiran P, Esmaillzadeh A, Azizi F (2007) Dietary diversity score and cardiovascular risk factors in Tehranian adults. Public Health Nutr 9(6):728–736. https://doi.org/10.1079/PHN2005887

    Article  Google Scholar 

  46. Livingstone KM, McNaughton SA (2016) Diet quality is associated with obesity and hypertension in Australian adults: a cross sectional study. BMC Public Health 16(1):1037. https://doi.org/10.1186/s12889-016-3714-5

    Article  PubMed  PubMed Central  Google Scholar 

  47. Conklin AI, Monsivais P, Khaw K-T, Wareham NJ, Forouhi NG (2016) Dietary diversity, diet cost, and incidence of type 2 diabetes in the United Kingdom: a prospective cohort study. PLoS Med 13(7):e1002085

    Article  Google Scholar 

  48. Zhang Q, Chen X, Liu Z, Varma DS, Wan R, Zhao S (2017) Diet diversity and nutritional status among adults in southwest China. PLoS One 12(2):e0172406. https://doi.org/10.1371/journal.pone.0172406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Bhupathiraju SN, Wedick NM, Pan A, Manson JE, Rexrode KM, Willett WC, Rimm EB, Hu FB (2013) Quantity and variety in fruit and vegetable intake and risk of coronary heart disease. Am J Clin Nutr 98(6):1514–1523

    Article  CAS  Google Scholar 

  50. Oude Griep LM, Verschuren WM, Kromhout D, Ocke MC, Geleijnse JM (2012) Variety in fruit and vegetable consumption and 10-year incidence of CHD and stroke. Public Health Nutr 15(12):2280–2286. https://doi.org/10.1017/s1368980012000912

    Article  PubMed  Google Scholar 

  51. Conrad Z, Raatz S, Jahns L (2018) Greater vegetable variety and amount are associated with lower prevalence of coronary heart disease: National Health and Nutrition Examination Survey, 1999–2014. Nutr J 17(1):67

    Article  Google Scholar 

  52. Conrad Z, Thomson J, Jahns L (2018) Prospective analysis of vegetable amount and variety on the risk of all-cause and cause-specific mortality among US adults, 1999–2011. Nutrients 10(10):1377

    Article  Google Scholar 

  53. Tsoupras A, Lordan R, Zabetakis I (2018) Inflammation, not cholesterol, is a cause of chronic disease. Nutrients 10(5):604

    Article  Google Scholar 

  54. Hansson GK (2005) Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352(16):1685–1695

    Article  CAS  Google Scholar 

  55. Hoebeeck LI, Rietzschel ER, Langlois M, De Buyzere M, De Bacquer D, De Backer G, Maes L, Gillebert T, Huybrechts I (2011) The relationship between diet and subclinical atherosclerosis: results from the Asklepios Study. Eur J Clin Nutr 65:606. https://doi.org/10.1038/ejcn.2010.286

    Article  CAS  PubMed  Google Scholar 

  56. Danquah I, Galbete C, Meeks K, Nicolaou M, Klipstein-Grobusch K, Addo J, Aikins AD, Amoah SK, Agyei-Baffour P, Boateng D, Bedu-Addo G, Spranger J, Smeeth L, Owusu-Dabo E, Agyemang C, Mockenhaupt FP, Beune E, Schulze MB (2017) Food variety, dietary diversity, and type 2 diabetes in a multi-center cross-sectional study among Ghanaian migrants in Europe and their compatriots in Ghana: the RODAM study. Eur J Nutr. https://doi.org/10.1007/s00394-017-1538-4

    Article  PubMed  PubMed Central  Google Scholar 

  57. Althubaiti A (2016) Information bias in health research: definition, pitfalls, and adjustment methods. J Multidiscip Healthc 9:211–217. https://doi.org/10.2147/JMDH.S104807

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors wish to thank the staff at the Western Australian Data Linkage Branch; Hospital Morbidity Data Collection; Registry of Births, Deaths and Marriages; Victorian Department of Justice and Regulation; and the National Coronial Information System for their work on providing the data for this study.

Funding

The Perth Longitudinal Study of Aging in Women (PLSAW) study was funded by Healthway the Western Australian Health Promotion Foundation and by Project Grants 254627, 303169, and 572604 from the National Health and Medical Research Council (NHMRC) of Australia. The analysis was supported by an NHMRC of Australia Project Grant 1084922. NHMRC of Australia Fellowships supported the salaries of JRL and JMH. None of these funding agencies had any role in the conduct of the study; collection, management, analysis, or interpretation of the data; or the preparation, review or approval of the manuscript.

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LCB, JRL, MS, AD, RLP, and JMH: study concept and design; JRL, AD, KZ, WHL, PLT, and RLP: acquisition of data; LCB, RJW, and JMH: statistical analysis and interpretation of data; LCB: drafting of the manuscript; and all authors: critical revision of the manuscript for important intellectual content.

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Correspondence to Lauren C. Blekkenhorst.

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Blekkenhorst, L.C., Lewis, J.R., Bondonno, C.P. et al. Vegetable diversity in relation with subclinical atherosclerosis and 15-year atherosclerotic vascular disease deaths in older adult women. Eur J Nutr 59, 217–230 (2020). https://doi.org/10.1007/s00394-019-01902-z

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  • DOI: https://doi.org/10.1007/s00394-019-01902-z

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