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Genomics and personalized strategies in nutrition

Association of maternal dietary habits and ADIPOQ gene polymorphisms with the risk of congenital heart defects in offspring: a hospital-based case-control study

European Journal of Clinical Nutrition volume 76, pages 373–381 (2022)Cite this article

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Abstract

Objectives

To estimate the association of maternal ADIPOQ gene, dietary habits in early pregnancy, and their interactions with the risk of congenital heart defects (CHDs) in offspring.

Methods

A case-control study of 464 mothers of CHDs children and 504 mothers of healthy children was included. Maternal dietary habits and genetic polymorphisms of ADIPOQ were the main exposure of interest. Their independent effects and interactions in the development of CHDs were analyzed in our study.

Results

The excessive consumption of pickled vegetables (aOR = 1.58, 95%CI: 1.17–2.12), smoked foods (aOR = 1.84, 95%CI:1.34–2.52), barbecued foods (aOR = 1.62, 95%CI: 1.09–2.39), fish and shrimp (aOR = 0.37, 95%CI: 0.27–50), and milk products (aOR = 0.64, 95%CI: 0.51–80) had a significant association with total CHDs risk. The polymorphisms of ADIPOQ gene at rs1501299 (T/T vs G/G: aOR = 0.27, 95%CI: 0.14–50; G/T vs G/G: aOR = 0.67, 95%CI: 0.46–98) and rs2241766 (G/G vs T/T: aOR = 4.35, 95%CI: 2.23–8.51; T/G vs T/T: aOR = 2.23, 95%CI: 1.51–3.28) showed a significant association with total CHDs risk. Likewise, our results found that maternal dietary habits and ADIPOQ genetic variants also were significantly related to the risk of specific CHDs phenotypes. In addition, gene-diet interaction revealed significant associations between the ADIPOQ gene and maternal dietary habits with total CHDs.

Conclusions

Maternal dietary habits, ADIPOQ gene, and their interactions show a significant association with the risk of CHDs. However, our study has some limitations, thus our findings need to be taken with caution, which highlights that more studies are required to further corroborate our findings.

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References

  1. Triedman JK, Newburger JW. Trends in congenital heart disease the next decade. Circulation. 2016;133:2716–33.

    Article  PubMed  Google Scholar 

  2. Liu Y, Chen S, Zuhlke L, Black GC, Choy M, Li N, et al. Global birth prevalence of congenital heart defects 1970-2017: updated systematic review and meta-analysis of 260 studies. Int J Epidemiol. 2019;48:455–63.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ntiloudi D, Zegkos T, Bazmpani MA, Parcharidou D, Panagiotidis T, Hadjimiltiades S. et al. Pregnancy outcome in women with congenital heart disease: a single-center experience. Hellenic J Cardiol. 2018;59:155–9.

    Article  PubMed  Google Scholar 

  4. Ntiloudi D, Zegkos T, Koutsakis A, Giannakoulas G, Karvounis H. Pregnancy in Patients with congenital heart disease a contemporary challenge. Cardiol Rev. 2017;25:326–30.

    Article  PubMed  Google Scholar 

  5. van der Linde D, Konings EEM, Slager MA, Witsenburg M, Helbing WA, Takkenberg JJM, et al. Birth prevalence of congenital heart disease worldwide a systematic review and meta-analysis. J Am Coll Cardiol. 2011;58:2241–7.

    Article  PubMed  Google Scholar 

  6. Uzark K. Challenges of assessing quality of life in congenital heart disease globally. J Am Coll Cardiol. 2016;67:2246–8.

    Article  PubMed  Google Scholar 

  7. Zaidi S, Brueckner M. Genetics and genomics of congenital heart disease. Circulation Res. 2017;120:923–40.

    Article  CAS  PubMed  Google Scholar 

  8. van der Bom T, Zomer AC, Zwinderman AH, Meijboom FJ, Bouma BJ, Mulder BJ. The changing epidemiology of congenital heart disease. Nat Rev Cardiol. 2011;8:50–60.

    Article  PubMed  Google Scholar 

  9. Wang T, Chen L, Yang T, Huang P, Wang L, Zhao L, et al. Congenital heart disease and risk of cardiovascular disease: a meta-analysis of cohort studies. J Am Heart Assoc. 2019;8:e012030.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Gaynor JW, Stopp C, Wypij DB, Andropoulos DB, Atallah J, Atz AM, et al. Neurodevelopmental outcomes after cardiac surgery in infancy. Pediatrics. 2015;135:816–25.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Jenkins KJ, Correa A, Feinstein JA, Botto L, Britt AE, Daniels SR, et al. Noninherited risk factors and congenital cardiovascular defects: current knowledge a scientific statement from the American heart association council on cardiovascular disease in the young. Circulation. 2007;115:2995–3014.

    Article  PubMed  Google Scholar 

  12. Wesołowska E, Jankowska A, Trafalska E, Kałużny P, Grzesiak M, Dominowska J, et al. Sociodemographic, lifestyle, environmental and pregnancy-related determinants of dietary patterns during pregnancy. Int J Environ Res Public Health. 2019;16:754.

    Article  PubMed Central  Google Scholar 

  13. Czeizel A, Dudás I, Vereczkey A, Bánhidy F. Folate deficiency and folic acid supplementation: the prevention of neural-tube defects and congenital heart defects. Nutrients. 2013;5:4760–75.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Smedts HPM, de Vries JH, Rakhshandehroo M, Wildhagen MF, Verkleij-Hagoort AC, Steegers EA, et al. High maternal vitamin E intake by diet or supplements is associated with congenital heart defects in the offspring. Obstetrical Gynecol Surv. 2009;64:301–2.

    Article  Google Scholar 

  15. Verkleij-Hagoort AC, de Vries JHM, Ursem NTC, de Jonge R, Hop WCJ, Steegers-Theunissen RPM. Dietary intake of B-vitamins in mothers born a child with a congenital heart defect. Eur J Nutr. 2006;45:478–86.

    Article  CAS  PubMed  Google Scholar 

  16. Shaw GM, Carmichael SL, Yang W, Lammer EJ. Periconceptional Nutrient intakes and risks of conotruncal heart defects. Birth Defects Res A Clin Mol Teratol. 2010;88:144–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Yang J, Kang Y, Cheng Y, Zeng L, Yan H, Dang S. Maternal dietary patterns during pregnancy and congenital heart defects: a case-control study. Int J Environ Res Public Health. 2019;16:2957.

    Article  CAS  PubMed Central  Google Scholar 

  18. Hu FB. Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol. 2002;13:3–9.

    Article  CAS  PubMed  Google Scholar 

  19. Ramya K, Ayyappa KA, Ghosh S, Mohan V, Radha V. Genetic association of ADIPOQ gene variants with type 2 diabetes, obesity and serum adiponectin levels in south Indian population. Gene. 2013;532:253–62.

    Article  CAS  PubMed  Google Scholar 

  20. Alfaqih MA, Khader YS, Al-Dwairi AN, Alzoubi A, Al-Shboul O, Hatim A. Lower levels of serum adiponectin and the T allele of rs1501299 of the ADIPOQ gene are protective against polycystic ovarian syndrome in Jordan. Korean J Fam Med. 2018;39:108–13.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Smetnev S, Klimushina M, Kutsenko V, Kiseleva A, Gumanova N, Kots A, et al. Associations of SNPs of the ADIPOQ gene with serum adiponectin levels, unstable angina, and coronary artery disease. Biomolecules. 2019;9:537.

    Article  PubMed Central  Google Scholar 

  22. Hivert MF, Manning AK, McAteer JB, Florez JC, Dupuis J, Fox CS, et al. Common variants in the adiponectin gene (ADIPOQ) associated with plasma adiponectin levels, type 2 diabetes, and diabetes-related quantitative traits: the Framingham offspring study. Diabetes. 2008;57:3353–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ong KL, Li M, Tso AW, Xu A, Cherny SS, Sham PC, et al. Association of genetic variants in the adiponectin gene with adiponectin level and hypertension in Hong Kong Chinese. Eur J Endocrinol. 2010;163:251–7.

    Article  CAS  PubMed  Google Scholar 

  24. Chu H, Wang M, Zhong D, Shi D, Ma L, Tong N, et al. AdipoQ polymorphisms are associated with type 2 diabetes mellitus: a meta-analysis study. Diabetes Metab Res Rev. 2013;29:532–45.

    CAS  PubMed  Google Scholar 

  25. Du J, Ye X, Li Q, Yu X, Cheng J, Ma J, et al. Genetic variants in the ADIPOQ gene and the risk of metabolic syndrome: a case-control study of a Chinese Han population. Ann Hum Genet. 2012;76:101–9.

    Article  CAS  PubMed  Google Scholar 

  26. Du W, Li Q, Lu Y, Yu X, Ye X, Gao Y, et al. Genetic variants in ADIPOQ gene and the risk of type 2 diabetes: a case-control study of Chinese Han population. Endocrine. 2011;40:413–22.

    Article  CAS  PubMed  Google Scholar 

  27. Chen L, Yang T, Chen L, Wang L, Wang T, Zhao L, et al. Risk of congenital heart defects in offspring exposed to maternal diabetes mellitus: an updated systematic review and meta-analysis. Arch Gynecol Obstet. 2019;300:1491–506.

    Article  PubMed  Google Scholar 

  28. Feng Y, Jiang CD, Chang AM, Shi Y, Gao J, Zhu L, et al. Interactions among insulin resistance, inflammation factors, obesity-related gene polymorphisms, environmental risk factors, and diet in the development of gestational diabetes mellitus. J Matern Fetal Neonatal Med. 2019;32:339–47.

    Article  CAS  PubMed  Google Scholar 

  29. Dietrich S, Jacobs S, Zheng JS, Meidtner K, Schwingshackl L, Schulze MB. Gene-lifestyle interaction on risk of type 2 diabetes: a systematic review. Obes Rev. 2019;20:1557–71.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Retamoso VR, Maurer P, Feijoo LB, Tavares G, Manfredini V, Piccoli J. ADIPOQ + 45T>/=G polymorphism, food ingestion, and metabolic syndrome in elderly persons. J Am Coll Nutr. 2018;37:209–14.

    Article  CAS  PubMed  Google Scholar 

  31. Cheng Y, Yan H, Dibley MJ, Shen Y, Li Q, Zeng L. Validity and reproducibility of a semi-quantitative food frequency questionnaire for use among pregnant women in rural China. Asia Pac J Clin Nutr. 2008;17:166–77.

    CAS  PubMed  Google Scholar 

  32. Sotres-Alvarez D, Siega-Riz AM, Herring AH, Carmichael SL, Feldkamp ML, Hobbs CA, et al. Maternal dietary patterns are associated with risk of neural tube and congenital heart defects. Am J Epidemiol. 2013;177:1279–88.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kalaycioglu Z, Erim FB. Nitrate and nitrites in foods: worldwide regional distribution in view of their risks and benefits. J Agric Food Chem. 2019;67:7205–22.

    Article  PubMed  Google Scholar 

  34. Machha A, Schechter AN. Dietary nitrite and nitrate: a review of potential mechanisms of cardiovascular benefits. Eur J Nutr. 2011;50:293–303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Bondonno CP, Croft KD, Hodgson JM. Dietary nitrate, nitric oxide, and cardiovascular health. Crit Rev Food Sci Nutr. 2016;56:2036–52.

    Article  CAS  PubMed  Google Scholar 

  36. Li J, Jia W, Zhao Q. Excessive nitrite affects zebrafish valvulogenesis through yielding too much NO signaling. PLoS ONE. 2014;9:e92728.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Alpert M, Diamond F, Friedhoff AJ. Tremographic studies in Tardive Dyskinesia. Psychopharmacol Bull. 1976;12:5–7.

    CAS  PubMed  Google Scholar 

  38. Jedrychowski W, Perera FP, Tang D, Stigter L, Mroz E, Flak E, et al. Impact of barbecued meat consumed in pregnancy on birth outcomes accounting for personal prenatal exposure to airborne polycyclic aromatic hydrocarbons: birth cohort study in Poland. Nutrition. 2012;28:372–7.

    Article  CAS  PubMed  Google Scholar 

  39. Jules GE, Pratap S, Ramesh A, Hood DB. In utero exposure to benzo(A)pyrene predisposes offspring to cardiovascular dysfunction in later-life. Toxicology 2012;295:56–67.

    Article  CAS  PubMed  Google Scholar 

  40. Huang L, Wang C, Zhang Y, Li J, Zhong Y, Zhou Y, et al. Benzo[a]pyrene exposure influences the cardiac development and the expression of cardiovascular relative genes in Zebrafish (Danio Rerio) Embryos. Chemosphere 2012;87:369–75.

    Article  CAS  PubMed  Google Scholar 

  41. Lupo PJ, Symanski E, Langlois PH, Lawson CC, Malik S, Gilboa SM, et al. Maternal occupational exposure to polycyclic aromatic hydrocarbons and congenital heart defects among offspring in the national birth defects prevention study. Birth Defects Res. 2012;94:875–81.

    Article  CAS  Google Scholar 

  42. Li N, Mu Y, Liu Z, Deng Y, Guo Y, Zhang X, et al. Assessment of interaction between maternal polycyclic aromatic hydrocarbons exposure and genetic polymorphisms on the risk of congenital heart diseases. Sci Rep. 2018;8:3075.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Huang M, Jiao J, Wang J, Xia Z, Zhang Y. Characterization of acrylamide-induced oxidative stress and cardiovascular toxicity in zebrafish embryos. J Hazard Mater. 2018;347:451–60.

    Article  CAS  PubMed  Google Scholar 

  44. Mousavi Khaneghah A, Fakhri Y, Nematollahi A, Seilani F, Vasseghian Y. The concentration of acrylamide in different food products: a global systematic review, meta-analysis, and meta-regression. Food Rev. Int. 2020. https://doi.org/10.1080/87559129.2020.1791175.

  45. Olatunji OS, Opeolu BO, Fatoki OS, Ximba BJ. Concentration profile of selected polycyclic aromatic hydrocarbon (PAH) fractions in some processed meat and meat products. J Food Meas Charact. 2013;7:122–8.

    Article  Google Scholar 

  46. Zhang S, Wang L, Yang T, Chen L, Zhao L, Wang T, et al. Parental alcohol consumption and the risk of congenital heart diseases in offspring: an updated systematic review and meta-analysis. Eur J Prev Cardiol. 2020;27:410–21.

    Article  PubMed  Google Scholar 

  47. Zhao L, Chen L, Yang T, Wang L, Wang T, Zhang S, et al. Parental smoking and the risk of congenital heart defects in offspring: an updated meta-analysis of observational studies. Eur J Prev Cardiol. 2020;27:1284–93.

    Article  PubMed  Google Scholar 

  48. Pan X, Marklund M, Wu JH. Fish consumption for cardiovascular health: benefits from long-chain omega-3 fatty acids versus potential harms due to mercury. Heart. 2019;105:1384–5.

    Article  PubMed  Google Scholar 

  49. Chrysant SG, Chrysant GS. An update on the cardiovascular pleiotropic effects of milk and milk products. J Clin Hypertens. 2013;15:503–10.

    Article  Google Scholar 

  50. Woo JG, Dolan LM, Deka R, Kaushal RD, Shen Y, Pal P, et al. Interactions between noncontiguous haplotypes in the adiponectin gene ACDC are associated with plasma adiponectin. Diabetes. 2006;55:523–9.

    Article  CAS  PubMed  Google Scholar 

  51. Yuan HP, Sun L, Li XH, Che FG, Zhu XQ, Yang F, et al. Association of adiponectin polymorphism with metabolic syndrome risk and adiponectin level with stroke. Risk. 2016;6:31945.

    CAS  Google Scholar 

  52. Bunin GR, Gyllstrom ME, Brown JE, Kahn EB, Kushi LH. Recall of diet during a past pregnancy. Am J Epidemiol. 2001;154:1136–42.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank the colleagues working in the research group, all subjects who participated in our study, as well as the editors and reviewers who provide us with valuable comments.

Funding

This research was funded by Project Funded by National Natural Science Foundation Program of China (81803313, 81973137, and 82073653), Hunan Provincial Key Research and Development Program (2018SK2063 and 2018SK2062), China Postdoctoral Science Foundation (2020M682644), Hunan Provincial Science and Technology Talent Support Project (2020TJ-N07), Open Project from NHC Key Laboratory of Birth Defect for Research and Prevention (KF2020006), Natural Science Foundation of Hunan Province (2018JJ2551), and Science and Technology Planning Project of Guangdong Province (2020A1414010152).

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Authors and Affiliations

  1. Department of Epidemiology and Health Statistics, Xiangya School of Public Health, Central South University, Changsha, Hunan, China

    Senmao Zhang, Xiaoying Liu, Tubao Yang, Tingting Wang, Lizhang Chen & Jiabi Qin

  2. Hunan Provincial Key Laboratory of Clinical Epidemiology, Changsha, Hunan, China

    Senmao Zhang, Xiaoying Liu, Tubao Yang, Lizhang Chen & Jiabi Qin

  3. National Health Commission Key Laboratory for Birth Defect Research and Prevention, Changsha, Hunan, China

    Tingting Wang & Jiabi Qin

  4. Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, Guangdong, China

    Jiabi Qin

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  1. Senmao Zhang
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Contributions

Conceptualization, SMZ, XYL, TBY, and JBQ; Formal analysis, SMZ, XYL, TTW, and TBY; Funding acquisition, LZC and JBQ; investigation and methodology, SMZ and TTW; writing-original draft, SMZ, LZC, and JBQ; Writing- review and editing, SMZ, XYL, LZC, and JBQ. All authors have read and approved the final version of the manuscript to be published.

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Correspondence to Lizhang Chen or Jiabi Qin.

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Zhang, S., Liu, X., Yang, T. et al. Association of maternal dietary habits and ADIPOQ gene polymorphisms with the risk of congenital heart defects in offspring: a hospital-based case-control study. Eur J Clin Nutr 76, 373–381 (2022). https://doi.org/10.1038/s41430-021-00969-4

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