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Plant food intake is associated with lower cadmium body burden in middle-aged adults

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Abstract

Purpose

Dietary intake is a primary source of cadmium (Cd) exposure in the non-smoking population. Plant foods containing metal-binding plant compounds such as polyphenols, phytates, and phytochelatins may reduce Cd bioavailability and result in lower Cd body burden. In this study, we investigated the association between plant food intake and urinary creatinine-adjusted Cd (uCd), a well-established marker of Cd body burden.

Methods

Participants were from a cross-sectional sample of 1901 adults in the REasons for Geographic and Racial Differences in Stroke (REGARDS) cohort. Dietary intake was assessed with a food frequency questionnaire. We created a 12-point plant food score (PFS) based on reported intake across seven categories (fruits, vegetables, legumes, nuts/seeds, whole grains, tea, and wine). Higher scores indicated higher consumption and diversity of plant food intake. Multivariable linear regression models were used to estimate the association between PFS and uCd. Due to the influence of age and smoking on Cd status, stratified analyses were conducted.

Results

Mean PFS was 5.4 (SD 2.2) and mean uCd was 0.53 µg/g creatinine (SD 0.39). In adjusted models, PFS was not associated with uCd (p > 0.05). In stratified analyses, PFS was inversely associated with uCd (p = 0.047) with a 1-point higher PFS associated with 0.018 µg/g lower uCd among middle-aged (45–59) adults. No significant association was observed between PFS and uCd in older (≥ 60) adults. The association of PFS and uCd did not differ by smoking status.

Conclusion

Our findings suggest higher plant food intake is associated with lower Cd body burden in middle-aged but not older adults.

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References

  1. ATSDR, Faroon O, Ashizawa A, Wright S, Tucker P, Jenkins K, Ingerman L, Rudisill C (2012) Toxicological profile for cadmium. Atlanta, GA

  2. Satarug S, Vesey DA, Gobe GC (2017) Health risk assessment of dietary cadmium intake: do current guidelines indicate how much is safe? Environ Health Perspect 125(3):284–288. https://doi.org/10.1289/EHP108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Satarug S (2018) Dietary Cadmium Intake and Its Effects on Kidneys. Toxics 6(1). doi:https://doi.org/10.3390/toxics6010015

  4. Kim K, Melough MM, Vance TM, Noh H, Koo SI, Chun OK (2018) Dietary Cadmium Intake and Sources in the US. Nutrients 11 (1). doi:https://doi.org/10.3390/nu11010002

  5. Satarug S, Vesey DA, Gobe GC (2017) Current health risk assessment practice for dietary cadmium: data from different countries. Food Chem Toxicol 106(Pt A):430–445. https://doi.org/10.1016/j.fct.2017.06.013

    Article  CAS  PubMed  Google Scholar 

  6. Flanagan PR, McLellan JS, Haist J, Cherian G, Chamberlain MJ, Valberg LS (1978) Increased dietary cadmium absorption in mice and human subjects with iron deficiency. Gastroenterology 74(5 Pt 1):841–846

    Article  CAS  PubMed  Google Scholar 

  7. Kikuchi Y, Nomiyama T, Kumagai N, Dekio F, Uemura T, Takebayashi T, Nishiwaki Y, Matsumoto Y, Sano Y, Hosoda K, Watanabe S, Sakurai H, Omae K (2003) Uptake of cadmium in meals from the digestive tract of young non-smoking Japanese female volunteers. J Occup Health 45(1):43–52

    Article  CAS  PubMed  Google Scholar 

  8. Horiguchi H, Oguma E, Sasaki S, Miyamoto K, Ikeda Y, Machida M, Kayama F (2004) Comprehensive study of the effects of age, iron deficiency, diabetes mellitus, and cadmium burden on dietary cadmium absorption in cadmium-exposed female Japanese farmers. Toxicol Appl Pharmacol 196(1):114–123. https://doi.org/10.1016/j.taap.2003.11.024

    Article  CAS  PubMed  Google Scholar 

  9. Anjum NA, Hasanuzzaman M, Hossain MA, Thangavel P, Roychoudhury A, Gill SS, Rodrigo MA, Adam V, Fujita M, Kizek R, Duarte AC, Pereira E, Ahmad I (2015) Jacks of metal/metalloid chelation trade in plants-an overview. Front Plant Sci 6:192. https://doi.org/10.3389/fpls.2015.00192

    Article  PubMed  PubMed Central  Google Scholar 

  10. Schlemmer U, Frolich W, Prieto RM, Grases F (2009) Phytate in foods and significance for humans: food sources, intake, processing, bioavailability, protective role and analysis. Mol Nutr Food Res 53(Suppl 2):S330-375. https://doi.org/10.1002/mnfr.200900099

    Article  PubMed  Google Scholar 

  11. Olszowy M (2019) What is responsible for antioxidant properties of polyphenolic compounds from plants? Plant Physiol Biochem 144:135–143. https://doi.org/10.1016/j.plaphy.2019.09.039

    Article  CAS  PubMed  Google Scholar 

  12. Dennis KK, Liu KH, Uppal K, Go YM, Jones DP (2021) Distribution of phytochelatins, metal-binding compounds, in plant foods: a survey of commonly consumed fruits, vegetables, grains and legumes. Food Chem 339:128051. https://doi.org/10.1016/j.foodchem.2020.128051

    Article  CAS  PubMed  Google Scholar 

  13. Jadan-Piedra C, Chiocchetti GM, Clemente MJ, Velez D, Devesa V (2018) Dietary compounds as modulators of metals and metalloids toxicity. Crit Rev Food Sci Nutr 58(12):2055–2067. https://doi.org/10.1080/10408398.2017.1302407

    Article  CAS  PubMed  Google Scholar 

  14. Van Hoydonck PG, Temme EH, Schouten EG (2002) A dietary oxidative balance score of vitamin C, beta-carotene and iron intakes and mortality risk in male smoking Belgians. J Nutr 132(4):756–761. https://doi.org/10.1093/jn/132.4.756

    Article  PubMed  Google Scholar 

  15. Goodman M, Bostick RM, Dash C, Flanders WD, Mandel JS (2007) Hypothesis: oxidative stress score as a combined measure of pro-oxidant and antioxidant exposures. Ann Epidemiol 17(5):394–399. https://doi.org/10.1016/j.annepidem.2007.01.034

    Article  PubMed  Google Scholar 

  16. McCullough ML, Willett WC (2006) Evaluating adherence to recommended diets in adults: the Alternate Healthy Eating Index. Public Health Nutr 9(1A):152–157. https://doi.org/10.1079/phn2005938

    Article  PubMed  Google Scholar 

  17. Trichopoulou A, Costacou T, Bamia C, Trichopoulos D (2003) Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med 348(26):2599–2608. https://doi.org/10.1056/NEJMoa025039

    Article  PubMed  Google Scholar 

  18. Hu FB (2002) Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol 13(1):3–9. https://doi.org/10.1097/00041433-200202000-00002

    Article  CAS  PubMed  Google Scholar 

  19. Scientific Opinion of the Panel on Contaminants in the Food Chain on a request from the European Commission on cadmium in food (2009). The EFSA Journal 980:1–139

  20. Tellez-Plaza M, Navas-Acien A, Caldwell KL, Menke A, Muntner P, Guallar E (2012) Reduction in cadmium exposure in the United States population, 1988–2008: the contribution of declining smoking rates. Environ Health Perspect 120(2):204–209. https://doi.org/10.1289/ehp.1104020

    Article  CAS  PubMed  Google Scholar 

  21. Gunier RB, Horn-Ross PL, Canchola AJ, Duffy CN, Reynolds P, Hertz A, Garcia E, Rull RP (2013) Determinants and within-person variability of urinary cadmium concentrations among women in northern California. Environ Health Perspect 121(6):643–649. https://doi.org/10.1289/ehp.1205524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Romagnani P, Remuzzi G, Glassock R, Levin A, Jager KJ, Tonelli M, Massy Z, Wanner C, Anders HJ (2017) Chronic kidney disease. Nat Rev Dis Primers 3:17088. https://doi.org/10.1038/nrdp.2017.88

    Article  PubMed  Google Scholar 

  23. Gekle M (2017) Kidney and aging—A narrative review. Exp Gerontol 87(Pt B):153–155. https://doi.org/10.1016/j.exger.2016.03.013

    Article  CAS  PubMed  Google Scholar 

  24. Howard VJ, Cushman M, Pulley L, Gomez CR, Go RC, Prineas RJ, Graham A, Moy CS, Howard G (2005) The reasons for geographic and racial differences in stroke study: objectives and design. Neuroepidemiology 25(3):135–143. https://doi.org/10.1159/000086678

    Article  PubMed  Google Scholar 

  25. Gutierrez OM, Muntner P, Rizk DV, McClellan WM, Warnock DG, Newby PK, Judd SE (2014) Dietary patterns and risk of death and progression to ESRD in individuals with CKD: a cohort study. Am J Kidney Dis 64(2):204–213. https://doi.org/10.1053/j.ajkd.2014.02.013

    Article  PubMed  PubMed Central  Google Scholar 

  26. Newby PK, Noel SE, Grant R, Judd S, Shikany JM, Ard J (2012) Race and region have independent and synergistic effects on dietary intakes in black and white women. Nutr J 11:25. https://doi.org/10.1186/1475-2891-11-25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chen C, Xun P, Tsinovoi C, McClure LA, Brockman J, MacDonald L, Cushman M, Cai J, Kamendulis L, Mackey J, He K (2018) Urinary cadmium concentration and the risk of ischemic stroke. Neurology 91(4):e382–e391. https://doi.org/10.1212/WNL.0000000000005856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Bowman SA, Friday JE, Moshfegh AJ (2008) MyPyramid Equivalents Database, 2.0 for USDA Survey Foods, 2003–2004: Documentation and User Guide.

  29. Byrd DA, Judd SE, Flanders WD, Hartman TJ, Fedirko V, Bostick RM (2019) Development and Validation of Novel Dietary and Lifestyle Inflammation Scores. J Nutr 149(12):2206–2218. https://doi.org/10.1093/jn/nxz165

    Article  PubMed  PubMed Central  Google Scholar 

  30. CDC (2007) NHANES 2003–2004: Data Documentation, Codebook, and Frequencies [Internet].

  31. Jarrett JM, Xiao G, Caldwell KL, Henahan D, Shakirova G, Jones RL (2008) Eliminating molybdenum oxide interference in urine cadmium biomonitoring using ICP-DRC-MS. J Anal At Spectrom 23:962–967

    Article  CAS  Google Scholar 

  32. McElroy JA, Kruse RL, Guthrie J, Gangnon RE, Robertson JD (2017) Cadmium exposure and endometrial cancer risk: a large midwestern US population-based case-control study. PLoS ONE 12(7):e0179360. https://doi.org/10.1371/journal.pone.0179360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Aaron KJ, Campbell RC, Judd SE, Sanders PW, Muntner P (2011) Association of dietary sodium and potassium intakes with albuminuria in normal-weight, overweight, and obese participants in the reasons for geographic and racial differences in stroke (REGARDS) study. Am J Clin Nutr 94(4):1071–1078. https://doi.org/10.3945/ajcn.111.013094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J, Ckd EPI (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150(9):604–612. https://doi.org/10.7326/0003-4819-150-9-200905050-00006

    Article  PubMed  PubMed Central  Google Scholar 

  35. Barr DB, Wilder LC, Caudill SP, Gonzalez AJ, Needham LL, Pirkle JL (2005) Urinary creatinine concentrations in the US population: implications for urinary biologic monitoring measurements. Environ Health Perspect 113(2):192–200. https://doi.org/10.1289/ehp.7337

    Article  CAS  PubMed  Google Scholar 

  36. R Core Team (2019) R: A Language and Environment for Statistical Computing.

  37. Wakimoto P, Block G (2001) Dietary intake, dietary patterns, and changes with age: an epidemiological perspective. J Gerontol A Biol Sci Med Sci 56 Spec No 2:65–80. doi:https://doi.org/10.1093/gerona/56.suppl_2.65

  38. Shlisky J, Bloom DE, Beaudreault AR, Tucker KL, Keller HH, Freund-Levi Y, Fielding RA, Cheng FW, Jensen GL, Wu D, Meydani SN (2017) Nutritional considerations for healthy aging and reduction in age-related chronic disease. Adv Nutr 8(1):17–26. https://doi.org/10.3945/an.116.013474

    Article  PubMed  PubMed Central  Google Scholar 

  39. Ervin RB (2008) Healthy Eating Index scores among adults, 60 years of age and over, by sociodemographic and health characteristics: United States, 1999–2002. Adv Data 395:1–16

    Google Scholar 

  40. Remond D, Shahar DR, Gille D, Pinto P, Kachal J, Peyron MA, Dos Santos CN, Walther B, Bordoni A, Dupont D, Tomas-Cobos L, Vergeres G (2015) Understanding the gastrointestinal tract of the elderly to develop dietary solutions that prevent malnutrition. Oncotarget 6(16):13858–13898. https://doi.org/10.18632/oncotarget.4030

    Article  PubMed  PubMed Central  Google Scholar 

  41. Gallagher CM, Kovach JS, Meliker JR (2008) Urinary cadmium and osteoporosis in U.S. Women > or= 50 years of age: NHANES 1988–1994 and 1999–2004. Environ Health Perspect 116 (10):1338–1343. doi:https://doi.org/10.1289/ehp.11452

  42. Tellez-Plaza M, Navas-Acien A, Menke A, Crainiceanu CM, Pastor-Barriuso R, Guallar E (2012) Cadmium exposure and all-cause and cardiovascular mortality in the US general population. Environ Health Perspect 120(7):1017–1022. https://doi.org/10.1289/ehp.1104352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. CDC (2019) Fourth Report on Human Exposure to Environmental Chemicals, Updated Tables. U.S. Department of Health and Human Services

  44. Riederer AM, Belova A, George BJ, Anastas PT (2013) Urinary cadmium in the 1999–2008 US national health and nutrition examination survey (NHANES). Environ Sci Technol 47(2):1137–1147. https://doi.org/10.1021/es303556n

    Article  CAS  PubMed  Google Scholar 

  45. Vacchi-Suzzi C, Eriksen KT, Levine K, McElroy J, Tjonneland A, Raaschou-Nielsen O, Harrington JM, Meliker JR (2015) Dietary intake estimates and urinary cadmium levels in danish postmenopausal women. PLoS ONE 10(9):e0138784. https://doi.org/10.1371/journal.pone.0138784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Copes R, Clark NA, Rideout K, Palaty J, Teschke K (2008) Uptake of cadmium from Pacific oysters (Crassostrea gigas) in British Columbia oyster growers. Environ Res 107(2):160–169. https://doi.org/10.1016/j.envres.2008.01.014

    Article  CAS  PubMed  Google Scholar 

  47. Sand S, Becker W (2012) Assessment of dietary cadmium exposure in Sweden and population health concern including scenario analysis. Food Chem Toxicol 50(3–4):536–544. https://doi.org/10.1016/j.fct.2011.12.034

    Article  CAS  PubMed  Google Scholar 

  48. Olmedo P, Grau-Perez M, Fretts A, Tellez-Plaza M, Gil F, Yeh F, Umans JG, Francesconi KA, Goessler W, Franceschini N, Lee ET, Best LG, Cole SA, Howard BV, Navas-Acien A (2017) Dietary determinants of cadmium exposure in the strong heart family study. Food Chem Toxicol 100:239–246. https://doi.org/10.1016/j.fct.2016.12.015

    Article  CAS  PubMed  Google Scholar 

  49. Vahter M, Berglund M, Nermell B, Akesson A (1996) Bioavailability of cadmium from shellfish and mixed diet in women. Toxicol Appl Pharmacol 136(2):332–341. https://doi.org/10.1006/taap.1996.0040

    Article  CAS  PubMed  Google Scholar 

  50. Berglund M, Akesson A, Nermell B, Vahter M (1994) Intestinal absorption of dietary cadmium in women depends on body iron stores and fiber intake. Environ Health Perspect 102(12):1058–1066. https://doi.org/10.1289/ehp.941021058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Taylor CM, Doerner R, Northstone K, Kordas K (2020) Maternal diet during pregnancy and blood cadmium concentrations in an observational cohort of British women. Nutrients 12 (4). doi:https://doi.org/10.3390/nu12040904

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Acknowledgements

The authors thank the other investigators, the staff, and the participants of the REGARDS study for their valuable contributions. A full list of participating REGARDS investigators and institutions can be found at http://www.uab.edu/soph/regardsstudy/.

Funding

The REGARDS research project is supported by a cooperative agreement U01 NS041588 co-funded by the National Institute of Neurological Disorders and Stroke (NINDS) and the National Institute on Aging (NIA), National Institutes of Health, Department of Health and Human Services. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NINDS or the NIA. Representatives of the NINDS were involved in the review of the manuscript but were not directly involved in the collection, management, analysis or interpretation of the data. Additional funding was provided by the National Institute of Environmental Health Sciences (NIEHS, R01 ES021735). Representatives from NIEHS did not have any role in the design and conduct of the study, the collection, management, analysis, and interpretation of the data, or the preparation or approval of the manuscript. The work of KD was supported by research grants from the NIH (T32 DK007734, F31 ES030980).

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Authors and Affiliations

  1. Nutrition and Health Sciences, Laney Graduate School, Emory University, Atlanta, GA, USA

    Kristine K. Dennis, Jessica A. Alvarez, Dean P. Jones & Terryl J. Hartman

  2. School of Public Health, University of Alabama at Birmingham, Birmingham, AL, USA

    Suzanne E. Judd

  3. Division of Endocrinology, Metabolism, and Lipids, Department of Medicine, Emory University, Atlanta, GA, USA

    Jessica A. Alvarez

  4. Epidemiology and Obstetrics and Gynecology, Columbia University Irving Medical Center, New York City, NY, USA

    Ka Kahe

  5. Division of Pulmonary, Allergy, and Critical Care Medicine, Department of Medicine, Emory University, Atlanta, GA, USA

    Dean P. Jones

  6. Department of Epidemiology, Rollins School of Public Health, Emory University, Atlanta, GA, USA

    Terryl J. Hartman

Authors
  1. Kristine K. Dennis
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  2. Suzanne E. Judd
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  3. Jessica A. Alvarez
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  4. Ka Kahe
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  5. Dean P. Jones
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  6. Terryl J. Hartman
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Contributions

All authors were responsible for the study conceptualization and design. KD was responsible for the data analysis. All authors contributed to the interpretation of the results. The manuscript was drafted by KD with input and critical revision from TH and DJ. All authors contributed to the final manuscript.

Corresponding author

Correspondence to Terryl J. Hartman.

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Dennis, K.K., Judd, S.E., Alvarez, J.A. et al. Plant food intake is associated with lower cadmium body burden in middle-aged adults. Eur J Nutr 60, 3365–3374 (2021). https://doi.org/10.1007/s00394-021-02513-3

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