Association of Manganese Biomarker Concentrations with Blood Pressure and Kidney Parameters among Healthy Adolescents: NHANES 2013–2018
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Population
2.2. Outcome Measurements
2.3. Exposure Measurements
2.4. Covariates
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Avila, D.S.; Puntel, R.L.; Aschner, M. Manganese in health and disease. Met. Ions Life Sci. 2013, 13, 199–227. [Google Scholar] [CrossRef]
- Sigel, A.; Sigel, H.; Sigel, R.K.O. Interrelations between Essential Metal Ions and Human Diseases; Springer: Dordrecht, The Netherlands, 2014. [Google Scholar]
- Balachandran, R.C.; Mukhopadhyay, S.; McBride, D.; Veevers, J.; Harrison, F.E.; Aschner, M.; Haynes, E.N.; Bowman, A.B. Brain manganese and the balance between essential roles and neurotoxicity. J. Biol. Chem. 2020, 295, 6312–6329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, P.; Tian, Y.; Xie, Q.; Zhang, L.; Yan, Y.; Xu, D. Manganese exposure induces permeability in renal glomerular endothelial cells via the Smad2/3-Snail-VE-cadherin axis. Toxicol. Res. (Camb.) 2020, 9, 683–692. [Google Scholar] [CrossRef]
- Sánchez-González, C.; López-Chaves, C.; Gómez-Aracena, J.; Galindo, P.; Aranda, P.; Llopis, J. Association of plasma manganese levels with chronic renal failure. J. Trace Elem. Med. Biol. 2015, 31, 78–84. [Google Scholar] [CrossRef]
- Liu, T.; Hivert, M.F.; Rifas-Shiman, S.L.; Rahman, M.L.; Oken, E.; Cardenas, A.; Mueller, N.T. Prospective Association Between Manganese in Early Pregnancy and the Risk of Preeclampsia. Epidemiology 2020, 31, 677–680. [Google Scholar] [CrossRef] [PubMed]
- Koh, E.S.; Kim, S.J.; Yoon, H.E.; Chung, J.H.; Chung, S.; Park, C.W.; Chang, Y.S.; Shin, S.J. Association of blood manganese level with diabetes and renal dysfunction: A cross-sectional study of the Korean general population. BMC Endocr. Disord. 2014, 14, 24. [Google Scholar] [CrossRef]
- Menezes-Filho, J.A.; Bouchard, M.; Sarcinelli Pde, N.; Moreira, J.C. Manganese exposure and the neuropsychological effect on children and adolescents: A review. Rev. Panam. Salud Publica 2009, 26, 541–548. [Google Scholar] [CrossRef] [Green Version]
- Cotzias, G.C.; Horiuchi, K.; Fuenzalida, S.; Mena, I. Chronic manganese poisoning. Clearance of tissue manganese concentrations with persistance of the neurological picture. Neurology 1968, 18, 376–382. [Google Scholar] [CrossRef] [PubMed]
- Schwartz, G.J.; Muñoz, A.; Schneider, M.F.; Mak, R.H.; Kaskel, F.; Warady, B.A.; Furth, S.L. New equations to estimate GFR in children with CKD. J. Am. Soc. Nephrol. 2009, 20, 629–637. [Google Scholar] [CrossRef] [Green Version]
- Centers for Disease Control and Prevention; National Center for Health Statistics. National Health and Nutrition Examination Survey Laboratory Protocol; Department of Health and Human Services, Centers for Disease Control and Prevention: Hyattsville, MD, USA, 2017.
- Chavers, B.M.; Simonson, J.; Michael, A.F. A solid phase fluorescent immunoassay for the measurement of human urinary albumin. Kidney Int. 1984, 25, 576–578. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rükgauer, M.; Klein, J.; Kruse-Jarres, J.D. Reference values for the trace elements copper, manganese, selenium, and zinc in the serum/plasma of children, adolescents, and adults. J. Trace Elem. Med. Biol. 1997, 11, 92–98. [Google Scholar] [CrossRef]
- Yang, J.; Yang, A.; Cheng, N.; Huang, W.; Huang, P.; Liu, N.; Bai, Y. Sex-specific associations of blood and urinary manganese levels with glucose levels, insulin resistance and kidney function in US adults: National health and nutrition examination survey 2011–2016. Chemosphere 2020, 258, 126940. [Google Scholar] [CrossRef]
- Pan, C.F.; Lin, C.J.; Chen, S.H.; Huang, C.F.; Lee, C.C. Association between trace element concentrations and anemia in patients with chronic kidney disease: A cross-sectional population-based study. J. Investig. Med. 2019, 67, 995–1001. [Google Scholar] [CrossRef] [PubMed]
- Melsom, T.; Nair, V.; Schei, J.; Mariani, L.; Stefansson, V.T.N.; Harder, J.L.; Jenssen, T.G.; Solbu, M.D.; Norvik, J.V.; Looker, H.; et al. Correlation Between Baseline GFR and Subsequent Change in GFR in Norwegian Adults Without Diabetes and in Pima Indians. Am. J Kidney Dis. 2019, 73, 777–785. [Google Scholar] [CrossRef] [Green Version]
- Thomson, H.J.; Ekinci, E.I.; Radcliffe, N.J.; Seah, J.M.; MacIsaac, R.J.; Jerums, G.; Premaratne, E. Elevated baseline glomerular filtration rate (GFR) is independently associated with a more rapid decline in renal function of patients with type 1 diabetes. J. Diabetes Complicat. 2016, 30, 256–261. [Google Scholar] [CrossRef]
- Jin, R.; Zhu, X.; Shrubsole, M.J.; Yu, C.; Xia, Z.; Dai, Q. Associations of renal function with urinary excretion of metals: Evidence from NHANES 2003–2012. Environ. Int. 2018, 121, 1355–1362. [Google Scholar] [CrossRef]
- Ferris, M.E.; Gipson, D.S.; Kimmel, P.L.; Eggers, P.W. Trends in treatment and outcomes of survival of adolescents initiating end-stage renal disease care in the United States of America. Pediatr. Nephrol. 2006, 21, 1020–1026. [Google Scholar] [CrossRef]
- Purnell, T.S.; Crews, D.C. Persistent Disparities in Preemptive Kidney Transplantation. Clin. J. Am. Soc. Nephrol. 2019, 14, 1430–1431. [Google Scholar] [CrossRef] [PubMed]
- Minnick, M.L.; Boynton, S.; Ndirangu, J.; Furth, S. Sex, race, and socioeconomic disparities in kidney disease in children. Semin. Nephrol. 2010, 30, 26–32. [Google Scholar] [CrossRef]
- Bankir, L.; Perucca, J.; Weinberger, M.H. Ethnic Differences in Urine Concentration: Possible Relationship to Blood Pressure. Clin. J. Am. Soc. Nephrol. 2007, 2, 304–312. [Google Scholar] [CrossRef]
- Jones, E.S.; Spence, J.D.; McIntyre, A.D.; Nondi, J.; Gogo, K.; Akintunde, A.; Hackam, D.G.; Rayner, B.L. High Frequency of Variants of Candidate Genes in Black Africans with Low Renin-Resistant Hypertension. Am. J. Hypertens. 2017, 30, 478–483. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johnson, J.A. Predictability of the effects of race or ethnicity on pharmacokinetics of drugs. Int. J. Clin. Pharmacol. Ther. 2000, 38, 53–60. [Google Scholar] [CrossRef]
- Bochud, M.; Staessen, J.A.; Maillard, M.; Mazeko, M.J.; Kuznetsova, T.; Woodiwiss, A.; Richart, T.; Norton, G.; Thijs, L.; Elston, R.; et al. Ethnic differences in proximal and distal tubular sodium reabsorption are heritable in black and white populations. J. Hypertens. 2009, 27, 606–612. [Google Scholar] [CrossRef] [Green Version]
- Sarić, M.; Hrustić, O. Exposure to airborne manganese and arterial blood pressure. Environ. Res. 1975, 10, 314–318. [Google Scholar] [CrossRef]
- Lee, B.K.; Kim, Y. Relationship between blood manganese and blood pressure in the Korean general population according to KNHANES 2008. Environ. Res. 2011, 111, 797–803. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.; Zheng, W. Cardiovascular toxicities upon manganese exposure. Cardiovasc. Toxicol. 2005, 5, 345–354. [Google Scholar] [CrossRef] [Green Version]
- Wu, C.; Woo, J.G.; Zhang, N. Association between urinary manganese and blood pressure: Results from National Health and Nutrition Examination Survey (NHANES), 2011-2014. PLoS ONE 2017, 12, e0188145. [Google Scholar] [CrossRef]
- O’Neal, S.L.; Zheng, W. Manganese Toxicity Upon Overexposure: A Decade in Review. Curr. Environ. Health Rep. 2015, 2, 315–328. [Google Scholar] [CrossRef] [Green Version]
- Oulhote, Y.; Mergler, D.; Bouchard, M.F. Sex-and age-differences in blood manganese levels in the U.S. general population: National health and nutrition examination survey 2011–2012. Environ. Health 2014, 13, 87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dees, W.L.; Hiney, J.K.; Srivastava, V.K. Influences of manganese on pubertal development. J. Endocrinol. 2017, 235, R33–R42. [Google Scholar] [CrossRef] [Green Version]
- Filler, G.; Qiu, Y.; Kaskel, F.; McIntyre, C.W. Principles responsible for trace element concentrations in chronic kidney disease. Clin. Nephrol. 2021, 96, 1–16. [Google Scholar] [CrossRef]
- Baker, M.G.; Simpson, C.D.; Stover, B.; Sheppard, L.; Checkoway, H.; Racette, B.A.; Seixas, N.S. Blood manganese as an exposure biomarker: State of the evidence. J. Occup. Environ. Hyg. 2014, 11, 210–217. [Google Scholar] [CrossRef] [Green Version]
- Choi, M.K.; Bae, Y.J. Dietary Intake and Urinary Excretion of Manganese in Korean Healthy Adults. Biol. Trace Elem. Res. 2020, 196, 384–392. [Google Scholar] [CrossRef] [PubMed]
- Klaassen, C.D. Biliary excretion of manganese in rats, rabbits, and dogs. Toxicol. Appl. Pharmacol. 1974, 29, 458–468. [Google Scholar] [CrossRef]
- Dastur, D.K.; Manghani, D.K.; Raghavendran, K.V.; Jeejeebhoy, K.N. Distribution and fate of Mn54 in the rat, with special reference to the C.N.S. Q. J. Exp. Physiol. Cogn. Med. Sci. 1969, 54, 322–331. [Google Scholar] [CrossRef] [PubMed]
- Laohaudomchok, W.; Lin, X.; Herrick, R.F.; Fang, S.C.; Cavallari, J.M.; Christiani, D.C.; Weisskopf, M.G. Toenail, blood, and urine as biomarkers of manganese exposure. J. Occup. Environ. Med. 2011, 53, 506–510. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Staples, A.; LeBlond, R.; Watkins, S.; Wong, C.; Brandt, J. Validation of the revised Schwartz estimating equation in a predominantly non-CKD population. Pediatr. Nephrol. 2010, 25, 2321–2326. [Google Scholar] [CrossRef] [PubMed]
- Levey, A.S.; Inker, L.A.; Coresh, J. GFR estimation: From physiology to public health. Am. J. Kidney Dis. 2014, 63, 820–834. [Google Scholar] [CrossRef] [Green Version]
- Pierce, C.B.; Muñoz, A.; Ng, D.K.; Warady, B.A.; Furth, S.L.; Schwartz, G.J. Age-and sex-dependent clinical equations to estimate glomerular filtration rates in children and young adults with chronic kidney disease. Kidney Int. 2021, 99, 948–956. [Google Scholar] [CrossRef]
N | % | |
---|---|---|
Sex | ||
Male | 962 | 49.8 |
Female | 969 | 50.2 |
Race/Ethnicity | ||
Mexican American | 399 | 20.7 |
Other Hispanic | 181 | 9.4 |
Non-Hispanic White | 604 | 31.3 |
Non-Hispanic Black | 386 | 20.0 |
Non-Hispanic Asian | 209 | 10.8 |
Other Race | 152 | 7.9 |
Family Poverty-Income Ratio | ||
<1 (low) | 570 | 29.6 |
≥1 (high) | 1361 | 70.4 |
Body Mass Index | ||
Underweight (z-score < −2) | 67 | 3.5 |
Normal (−2 ≤ z-score < 1) | 1081 | 56.0 |
Overweight (1 ≤ z-score < 2) | 337 | 17.4 |
Obese (z-score ≥ 2) | 446 | 23.1 |
Mean ± Standard Deviation | ||
Age (years) | 15.4 ± 2.2 | |
Blood Mn (µg/L) | 11.2 ± 3.9 | |
Urine Mn (µg/L) | 0.15 ± 0.17 | |
eGFR (mL/min/1.73 m2) | 100.4 ± 21.6 | |
SBP (mmHg) | 108.6 ± 9.6 | |
DBP (mmHg) | 60.7 ± 10.3 | |
BUN (mg/dL) | 11.4 ± 3.5 | |
ACR (mg/g) | 24.1 ± 89.2 |
Unadjusted | Adjusted 1 | |||||
---|---|---|---|---|---|---|
β | 95% CI | p-Value | β | 95% CI | p-Value | |
eGFR | 23.2 | (14.4, 32.0) | <0.0001 | 5.8 | (−1.6, 13.2) | 0.1 |
SBP | −3.8 | (−7.3, −0.4) | 0.03 | 0.4 | (−3.0, 3.8) | 0.8 |
DBP | −0.9 | (−5.6, 3.8) | 0.7 | −1.3 | (−6.0, 3.4) | 0.6 |
BUN | −1.3 | (−3.3, 0.6) | 0.2 | −0.03 | (−1.7, 1.6) | 0.9 |
ACR | 0.2 | (0.02, 0.4) | 0.03 | 0.04 | (−0.2, 0.2) | 0.7 |
Males | Females | |||||
---|---|---|---|---|---|---|
β | 95% CI | p-Value | β | 95% CI | p-Value | |
eGFR | 5.7 | (−5.9, 17.3) | 0.3 | 3.2 | (−8.0, 14.4) | 0.6 |
SBP | −0.6 | (−6.5, 5.3) | 0.8 | 1.4 | (−3.1, 6.0) | 0.5 |
DBP | 0.6 | (−8.2, 9.3) | 0.9 | −2.4 | (−8.6, 3.8) | 0.4 |
BUN | −0.7 | (−3.0, 1.5) | 0.5 | 0.7 | (−1.4, 2.8) | 0.5 |
ACR | 0.2 | (−0.2, 0.5) | 0.3 | −0.08 | (−0.3, 0.2) | 0.5 |
eGFR | SBP | DBP | BUN | ACR | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
β | 95% CI | p-Value | β | 95% CI | p-Value | β | 95% CI | p-Value | β | 95% CI | p-Value | β | 95% CI | p-Value | |
Mexican American | 5.7 | (−8.9, 20.4) | 0.4 | −1.05 | (−9.7, 7.6) | 0.8 | 4.52 | (−5.4, 14.5) | 0.4 | −0.47 | (−2.7, 1.8) | 0.7 | −0.2 | (−0.6, 0.3) | 0.4 |
Other Hispanic | 29.4 | (−0.4, 59.3) | 0.053 | −3.3 | (−13.0, 6.4) | 0.5 | 6.37 | (−6.5, 19.2) | 0.3 | 2.1 | (−2.6, 6.9) | 0.4 | 0.5 | (0.1, 1.0) | 0.01 |
Non-Hispanic White | −1.99 | (−12.8, 8.9) | 0.7 | 2.4 | (−2.9, 7.7) | 0.4 | −1.82 | (−8.6, 5.0) | 0.5 | 0.5 | (−2.0, 3.0) | 0.7 | 0.03 | (−0.3, 0.4) | 0.8 |
Non-Hispanic Black | 14.5 | (0.4, 28.7) | 0.04 | 5.9 | (−1.6, 13.4) | 0.1 | −4.76 | (−13.0, 3.6) | 0.2 | −1.03 | (−3.6, 1.7) | 0.4 | 0.1 | (−0.2, 0.4) | 0.3 |
Non-Hispanic Asian | 15.9 | (−33.6, 65.4) | 0.5 | 5.2 | (−2.5, 13.0) | 0.2 | −3.51 | (−14.7, 7.7) | 0.5 | −2.3 | (−6.4, 1.9) | 0.3 | −0.1 | (−0.5, 0.3) | 0.6 |
Other Race | 28.4 | (6.8, 50.1) | 0.01 | −23.8 | (−36.1, −11.6) | 0.0003 | −8.37 | (−26.9, 10.2) | 0.4 | 0.02 | (−3.1, 3.1) | 0.9 | −0.2 | (−0.7, 0.3) | 0.5 |
Unadjusted | Adjusted 1 | |||||
---|---|---|---|---|---|---|
β | 95% CI | p-Value | β | 95% CI | p-Value | |
eGFR | 19.5 | (14.4, 24.6) | <0.0001 | 16.4 | (11.1, 21.7) | <0.0001 |
SBP | −1.6 | (−4.0, 0.7) | 0.2 | 0.1 | (−2.1, 2.3) | 0.9 |
DBP | 1.7 | (−1.4, 1.5) | 0.3 | 0.4 | (−2.3, 3.1) | 0.8 |
BUN | −0.6 | (−1.5, 0.4) | 0.2 | −0.5 | (−1.3, 0.4) | 0.3 |
ACR | 0.07 | (−0.04, 0.2) | 0.2 | −0.02 | (−0.1, 0.1) | 0.8 |
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Politis, M.D.; Freedman, J.C.; Haynes, E.N.; Sanders, A.P. Association of Manganese Biomarker Concentrations with Blood Pressure and Kidney Parameters among Healthy Adolescents: NHANES 2013–2018. Children 2021, 8, 846. https://doi.org/10.3390/children8100846
Politis MD, Freedman JC, Haynes EN, Sanders AP. Association of Manganese Biomarker Concentrations with Blood Pressure and Kidney Parameters among Healthy Adolescents: NHANES 2013–2018. Children. 2021; 8(10):846. https://doi.org/10.3390/children8100846
Chicago/Turabian StylePolitis, Maria D., Jacob C. Freedman, Erin N. Haynes, and Alison P. Sanders. 2021. "Association of Manganese Biomarker Concentrations with Blood Pressure and Kidney Parameters among Healthy Adolescents: NHANES 2013–2018" Children 8, no. 10: 846. https://doi.org/10.3390/children8100846