Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-25T16:37:38.027Z Has data issue: false hasContentIssue false

Inverse correlations between serum carotenoids and respiratory morbidity and mortality: the Third National Health and Nutrition Examination Survey

Published online by Cambridge University Press:  11 April 2023

Ruiming Yang
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Ziteng Cao
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Xin Liu
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Mengjie Xiao
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Mengyao Li
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Yunyan Chen
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Luyao Chen
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Changhao Sun
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Xia Chu
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China
Qiang Ren
Affiliation:
Department of Respiratory Medicine, The First Affiliated Hospital of Harbin Medical University, Harbin, People’s Republic of China
Wei Wei*
Affiliation:
Department of Nutrition and Food Hygiene, The National Key Discipline, School of Public Health, Harbin Medical University, Harbin, People’s Republic of China Department of Pharmacology, College of Pharmacy Key Laboratory of Cardiovascular Research, Ministry of Education, Harbin Medical University, Harbin, People’s Republic of China
*
*Corresponding author: Wei Wei, email 102594@hrbmu.edu.cn

Abstract

The objective was to evaluate the association between serum carotenoid levels and respiratory morbidity and mortality in a nationally representative sample of US adults. We assessed the association of serum carotenoid levels with respiratory morbidity and mortality using logistic regression and proportional hazards regression models. Meanwhile, a series of confounders were controlled in regression models and restricted cubic spline, which included age, sex, race, marriage, education, income, drinking, smoking, regular exercise, BMI, daily energy intake, vitamin E, vitamin C, fruit intake, vegetable intake, diabetes, hypertension, asthma, emphysema and chronic bronchitis. Compared with participants in the lowest tertiles, participants in the highest tertiles of serum total carotenoids, β-cryptoxanthin and lutein/zeaxanthin levels had a significantly lower prevalence of emphysema (ORtotal carotenoids = 0·61, 95% CI: 0·41–0·89, ORβ-cryptoxanthin = 0·67, 95% CI: 0·49–0·92), chronic bronchitis (ORβ-cryptoxanthin = 0·66, 95% CI: 0·50–0·87) and asthma (Q2: ORlutein/zeaxanthin = 0·78, 95% CI: 0·62–0·97); participants in the highest tertiles of total carotenoids, α-carotene, lutein/zeaxanthin and lycopene had a lower risk of respiratory mortality (hazard ratio (HR)total carotenoids = 0·62, 95% CI: 0·42–0·90, HRα-carotene = 0·54, 95% CI: 0·36–0·82, HRlutein/zeaxanthin = 0·48, 95% CI: 0·33–0·71, HRlycopene = 0·66, 95% CI: 0·45–0·96) than those in the lowest tertiles. Higher serum total carotenoids and β-cryptoxanthin levels is associated with decreased prevalence of emphysema and chronic bronchitis, and higher serum total carotenoids, α-carotene, lutein/zeaxanthin and lycopene levels had a lower mortality of respiratory disease.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

These authors contributed equally to this work

References

Pisoschi, AM & Pop, A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97, 5574.CrossRefGoogle ScholarPubMed
Kattoor, AJ, Pothineni, NVK, Palagiri, D, et al. (2017) Oxidative stress in atherosclerosis. Curr Atheroscler Rep 19, 42.CrossRefGoogle Scholar
Sztretye, M, Dienes, B, Gönczi, M, et al. (2019) Astaxanthin: a potential mitochondrial-targeted antioxidant treatment in diseases and with aging. Oxid Med Cell Longev 2019, 3849692.CrossRefGoogle ScholarPubMed
Saleem, U, Sabir, S, Niazi, SG, et al. (2020) Role of oxidative stress and antioxidant defense biomarkers in neurodegenerative diseases. Crit Rev Eukaryot Gene Expr 30, 311322.CrossRefGoogle ScholarPubMed
Liguori, I, Russo, G, Curcio, F, et al. (2018) Oxidative stress, aging, and diseases. Clin Interv Aging 13, 757772.CrossRefGoogle ScholarPubMed
Johra, FT, Bepari, AK, Bristy, AT, et al. (2020) A mechanistic review of β-carotene, lutein, and zeaxanthin in eye health and disease. Antioxidants 9, 1046.CrossRefGoogle ScholarPubMed
Fan, S, Sun, JB, Li, R, et al. (2019) Lycopene protects myocardial ischemia injury through anti-apoptosis and anti-oxidative stress. Eur Rev Med Pharmacol Sci 23, 30963104.Google ScholarPubMed
Tang, C, Xie, J, Lv, J, et al. (2021) Alleviating damage of photosystem and oxidative stress from chilling stress with exogenous zeaxanthin in pepper (Capsicum annuum L.) seedlings. Plant Physiol Biochem 162, 395409.CrossRefGoogle ScholarPubMed
Liu, XR, Wang, YY, Fan, HR, et al. (2016) Preventive effects of β-cryptoxanthin against cadmium-induced oxidative stress in the rat testis. Asian J Androl 18, 920924.Google ScholarPubMed
Du, C, Lv, T, Liu, Q, et al. (2021) Carotenoids in Sporidiobolus pararoseus ameliorate diabetic nephropathy in mice through attenuating oxidative stress. Biol Chem 402, 785794.CrossRefGoogle ScholarPubMed
Bohn, T (2019) Carotenoids and markers of oxidative stress in human observational studies and intervention trials: implications for chronic diseases. Antioxidants 8, 179.CrossRefGoogle ScholarPubMed
Yeum, KJ & Russell, RM (2002) Carotenoid bioavailability and bioconversion. Annu Rev Nutr 22, 483504.CrossRefGoogle ScholarPubMed
Milani, A, Basirnejad, M, Shahbazi, S, et al. (2017) Carotenoids: biochemistry, pharmacology and treatment. Br J Pharmacol 174, 12901324.CrossRefGoogle ScholarPubMed
Rogers, LK & Cismowski, MJ (2018) Oxidative stress in the lung – the essential paradox. Curr Opin Toxicol 7, 3743.CrossRefGoogle ScholarPubMed
Cannavò, L, Perrone, S, Viola, V, et al. (2021) Oxidative stress and respiratory diseases in preterm newborns. Int J Mol Sci 22, 12504.CrossRefGoogle ScholarPubMed
Virtamo, J, Taylor, PR, Kontto, J, et al. (2014) Effects of α-tocopherol and β-carotene supplementation on cancer incidence and mortality: 18-year postintervention follow-up of the Alpha-tocopherol, Beta-carotene Cancer Prevention Study. Int J Cancer 135, 178185.CrossRefGoogle ScholarPubMed
Wiegman, CH, Li, F, Ryffel, B, et al. (2020) Oxidative stress in ozone-induced chronic lung inflammation and emphysema: a facet of chronic obstructive pulmonary disease. Front Immunol 11, 1957.CrossRefGoogle ScholarPubMed
Liu, K, Hua, S & Song, L (2022) PM2.5 exposure and asthma development: the key role of oxidative stress. Oxid Med Cell Longev 2022, 3618806.Google ScholarPubMed
Thomson, CA, Stendell-Hollis, NR, Rock, CL, et al. (2007) Plasma and dietary carotenoids are associated with reduced oxidative stress in women previously treated for breast cancer. Cancer Epidemiol Biomarkers Prev 16, 20082015.CrossRefGoogle ScholarPubMed
Gammone, MA, Riccioni, G & D’Orazio, N (2015) Marine carotenoids against oxidative stress: effects on human health. Mar Drugs 13, 62266246.CrossRefGoogle ScholarPubMed
Genç, Y, Bardakci, H, Yücel, Ç, et al. (2020) Oxidative stress and marine carotenoids: application by using nanoformulations. Mar Drugs 18, 423.CrossRefGoogle ScholarPubMed
Amengual, J, Lobo, GP, Golczak, M, et al. (2011) A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB J 25, 948959.CrossRefGoogle ScholarPubMed
Borel, P, Grolier, P, Boirie, Y, et al. (1998) Oxidative stress status and antioxidant status are apparently not related to carotenoid status in healthy subjects. J Lab Clin Med 132, 6166.CrossRefGoogle Scholar
Zhang, W, Li, W & Du, J (2022) Association between dietary carotenoid intakes and the risk of asthma in adults: a cross-sectional study of NHANES, 2007–2012. BMJ Open 12, e052320.CrossRefGoogle ScholarPubMed
Min, KB & Min, JY (2014) Serum carotenoid levels and risk of lung cancer death in US adults. Cancer Sci 105, 736743.CrossRefGoogle ScholarPubMed
Gunter, EW, Lewis, BL & Koncikowski, SM (1996) Laboratory Methods used for the Third National Health and Nutrition Examination Survey (NHANES III), 1988–1994. Atlanta, GA: US Department of Health and Human Services.Google Scholar
Wood, LG, Garg, ML, Blake, RJ, et al. (2005) Airway and circulating levels of carotenoids in asthma and healthy controls. J Am Coll Nutr 24, 448455.CrossRefGoogle ScholarPubMed
Wood, LG & Gibson, PG (2010) Reduced circulating antioxidant defences are associated with airway hyper-responsiveness, poor control and severe disease pattern in asthma. Br J Nutr 103, 735741.CrossRefGoogle ScholarPubMed
Eggersdorfer, M & Wyss, A (2018) Carotenoids in human nutrition and health. Arch Biochem Biophys 652, 1826.CrossRefGoogle ScholarPubMed
Kaulmann, A, Jonville, MC, Schneider, YJ, et al. (2014) Carotenoids, polyphenols and micronutrient profiles of Brassica oleraceae and plum varieties and their contribution to measures of total antioxidant capacity. Food Chem 155, 240250.CrossRefGoogle ScholarPubMed
Nakano, T, Tanaka, S, Tsuruya, K, et al. (2022) Low intake of β carotene and dietary fiber from vegetables and fruits in patients with chronic kidney disease. Sci Rep 12, 19953.CrossRefGoogle ScholarPubMed
Böhm, V, Lietz, G, Olmedilla-Alonso, B, et al. (2021) From carotenoid intake to carotenoid blood and tissue concentrations – implications for dietary intake recommendations. Nutr Rev 79, 544573.CrossRefGoogle ScholarPubMed
Manochkumar, J, Doss, CGP, El-Seedi, HR, et al. (2021) The neuroprotective potential of carotenoids in vitro and in vivo . Phytomedicine 91, 153676.CrossRefGoogle ScholarPubMed
Dianat, M, Radan, M, Badavi, M, et al. (2018) Crocin attenuates cigarette smoke-induced lung injury and cardiac dysfunction by anti-oxidative effects: the role of Nrf2 antioxidant system in preventing oxidative stress. Respir Res 19, 58.CrossRefGoogle ScholarPubMed
Kodama, Y, Kishimoto, Y, Muramatsu, Y, et al. (2017) Antioxidant nutrients in plasma of Japanese patients with chronic obstructive pulmonary disease, asthma-COPD overlap syndrome and bronchial asthma. Clin Respir J 11, 915924.CrossRefGoogle ScholarPubMed
Campos, KKD, de Oliveira Ramos, C, Martins, TL, et al. (2019) Lycopene mitigates pulmonary emphysema induced by cigarette smoke in a murine model. J Nutr Biochem 65, 93100.CrossRefGoogle ScholarPubMed
Jun, L & Root, M (2021) Association of carotenoid intake with pulmonary function. J Am Coll Nutr 40, 708712.CrossRefGoogle ScholarPubMed
Pérez-Torres, I, Castrejón-Téllez, V, Soto, ME, et al. (2021) Oxidative stress, plant natural antioxidants, and obesity. Int J Mol Sci 22, 1786.CrossRefGoogle ScholarPubMed
Jakubiak, GK, Osadnik, K, Lejawa, M, et al. (2021) Oxidative stress in association with metabolic health and obesity in young adults. Oxid Med Cell Longev 2021, 9987352.CrossRefGoogle ScholarPubMed
Grasemann, H & Holguin, F (2021) Oxidative stress and obesity-related asthma. Paediatr Respir Rev 37, 1821.Google ScholarPubMed
Handelman, GJ, Packer, L & Cross, CE (1996) Destruction of tocopherols, carotenoids, and retinol in human plasma by cigarette smoke. Am J Clin Nutr 63, 559565.CrossRefGoogle ScholarPubMed
Iskandar, AR, Liu, C, Smith, DE, et al. (2013) β-cryptoxanthin restores nicotine-reduced lung SIRT1 to normal levels and inhibits nicotine-promoted lung tumorigenesis and emphysema in A/J mice. Cancer Prev Res 6, 309320.CrossRefGoogle ScholarPubMed
Hemilä, H, Virtamo, J, Albanes, D, et al. (2004) Vitamin E and beta-carotene supplementation and hospital-treated pneumonia incidence in male smokers. Chest 125, 557565.CrossRefGoogle ScholarPubMed
Schünemann, HJ, McCann, S, Grant, BJ, et al. (2002) Lung function in relation to intake of carotenoids and other antioxidant vitamins in a population-based study. Am J Epidemiol 155, 463471.CrossRefGoogle ScholarPubMed
Mustra Rakic, J, Liu, C, Veeramachaneni, S, et al. (2019) Lycopene inhibits smoke-induced chronic obstructive pulmonary disease and lung carcinogenesis by modulating reverse cholesterol transport in ferrets. Cancer Prev Res 12, 421432.CrossRefGoogle ScholarPubMed
Kentson, M, Leanderson, P, Jacobson, P, et al. (2018) Oxidant status, iron homeostasis, and carotenoid levels of COPD patients with advanced disease and LTOT. Eur Clin Respir J 5, 1447221.CrossRefGoogle ScholarPubMed
Supplementary material: File

Yang et al. supplementary material

Tables S1-S9

Download Yang et al. supplementary material(File)
File 163.3 KB