Positive Association of Urinary Dimethylarsinic Acid (DMAV) with Serum 25(OH)D in Adults Living in an Area of Water-Borne Arsenicosis in Shanxi, China
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Site and Population
2.2. Sample Collection
2.3. Determination of Urinary Arsenic Concentrations
2.4. Determination of Serum 25(OH)D Concentrations
2.5. Determination of Blood Glucose Concentrations
2.6. Quality Assurance and Quality Control
2.7. Statistical Analysis
3. Results
3.1. Basic Characteristics of the Study Population
3.2. Multivariate Linear Regression Analysis between Urinary Arsenic Species and Serum 25(OH)D
3.3. Associations between Urinary Arsenic Species and Vitamin D Status
3.4. Association between Arsenic Metabolism Efficiency and Serum Vitamin D
3.5. Association between Urinary Arsenic Species and Serum 25 (OH)D in Subgroups Stratified by Skin Hyperkeratosis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Reid, I.R.; Bolland, M.J.; Grey, A. Effects of vitamin D supplements on bone mineral density: A systematic review and meta-analysis. Lancet 2014, 383, 146–155. [Google Scholar] [CrossRef]
- Wilson, L.R.; Tripkovic, L.; Hart, K.H.; Lanham-New, S.A. Vitamin D deficiency as a public health issue: Using vitamin D2 or vitamin D3 in future fortification strategies. Proc. Nutr. Soc. 2017, 76, 392–399. [Google Scholar] [CrossRef]
- Prietl, B.; Treiber, G.; Pieber, T.R.; Amrein, K. Vitamin D and immune function. Nutrients 2013, 5, 2502–2521. [Google Scholar] [CrossRef]
- Heaney, R.P. Vitamin D in health and disease. Clin. J. Am. Soc. Nephrol. CJASN 2008, 3, 1535–1541. [Google Scholar] [CrossRef]
- Ormsby, R.T.; Findlay, D.M.; Kogawa, M.; Anderson, P.H.; Morris, H.A.; Atkins, G.J. Analysis of vitamin D metabolism gene expression in human bone: Evidence for autocrine control of bone remodelling. J. Steroid Biochem. Mol. Biol. 2014, 144 Pt A, 110–113. [Google Scholar] [CrossRef]
- Holick, M.F. The vitamin D deficiency pandemic: Approaches for diagnosis, treatment and prevention. Rev. Endocr. Metab. Disord. 2017, 18, 153–165. [Google Scholar] [CrossRef]
- Rosen, C.J.; Taylor, C.L. Common misconceptions about vitamin D—Implications for clinicians. Nat. Rev. Endocrinol. 2013, 9, 434–438. [Google Scholar] [CrossRef]
- Alshahrani, F.; Aljohani, N. Vitamin D: Deficiency, sufficiency and toxicity. Nutrients 2013, 5, 3605–3616. [Google Scholar] [CrossRef]
- Holick, M.F. Vitamin D deficiency. N. Engl. J. Med. 2007, 357, 266–281. [Google Scholar] [CrossRef]
- Nair, P.; Venkatesh, B.; Center, J.R. Vitamin D deficiency and supplementation in critical illness-the known knowns and known unknowns. Crit. Care 2018, 22, 276. [Google Scholar] [CrossRef]
- Marcinowska-Suchowierska, E.; Kupisz-Urbańska, M.; Łukaszkiewicz, J.; Płudowski, P.; Jones, G. Vitamin D Toxicity-A Clinical Perspective. Front. Endocrinol. 2018, 9, 550. [Google Scholar] [CrossRef]
- Tsiaras, W.G.; Weinstock, M.A. Factors influencing vitamin D status. Acta Derm.-Venereol. 2011, 91, 115–124. [Google Scholar] [CrossRef]
- Meza-Meza, M.R.; Ruiz-Ballesteros, A.I.; de la Cruz-Mosso, U. Functional effects of vitamin D: From nutrient to immunomodulator. Crit. Rev. Food Sci. Nutr. 2022, 62, 3042–3062. [Google Scholar] [CrossRef]
- Mousavi, S.E.; Amini, H.; Heydarpour, P.; Amini Chermahini, F.; Godderis, L. Air pollution, environmental chemicals, and smoking may trigger vitamin D deficiency: Evidence and potential mechanisms. Environ. Int. 2019, 122, 67–90. [Google Scholar] [CrossRef]
- Barrea, L.; Savastano, S.; Di Somma, C.; Savanelli, M.C.; Nappi, F.; Albanese, L.; Orio, F.; Colao, A. Low serum vitamin D-status, air pollution and obesity: A dangerous liaison. Rev. Endocr. Metab. Disord. 2017, 18, 207–214. [Google Scholar] [CrossRef]
- Hoseinzadeh, E.; Taha, P.; Wei, C.; Godini, H.; Ashraf, G.M.; Taghavi, M.; Miri, M. The impact of air pollutants, UV exposure and geographic location on vitamin D deficiency. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 2018, 113, 241–254. [Google Scholar] [CrossRef]
- Bimonte, V.M.; Besharat, Z.M.; Antonioni, A.; Cella, V.; Lenzi, A.; Ferretti, E.; Migliaccio, S. The endocrine disruptor cadmium: A new player in the pathophysiology of metabolic diseases. J. Endocrinol. Investig. 2021, 44, 1363–1377. [Google Scholar] [CrossRef]
- Nogawa, K.; Tsuritani, I.; Kido, T.; Honda, R.; Yamada, Y.; Ishizaki, M. Mechanism for bone disease found in inhabitants environmentally exposed to cadmium: Decreased serum 1 alpha, 25-dihydroxyvitamin D level. Int. Arch. Occup. Environ. Health 1987, 59, 21–30. [Google Scholar] [CrossRef]
- Nogawa, K.; Tsuritani, I.; Kido, T.; Honda, R.; Ishizaki, M.; Yamada, Y. Serum vitamin D metabolites in cadmium-exposed persons with renal damage. Int. Arch. Occup. Environ. Health 1990, 62, 189–193. [Google Scholar] [CrossRef]
- Arbuckle, T.E.; Liang, C.L.; Morisset, A.S.; Fisher, M.; Weiler, H.; Cirtiu, C.M.; Legrand, M.; Davis, K.; Ettinger, A.S.; Fraser, W.D. Maternal and fetal exposure to cadmium, lead, manganese and mercury: The MIREC study. Chemosphere 2016, 163, 270–282. [Google Scholar] [CrossRef]
- Rosen, J.F.; Chesney, R.W.; Hamstra, A.; DeLuca, H.F.; Mahaffey, K.R. Reduction in 1,25-dihydroxyvitamin D in children with increased lead absorption. N. Engl. J. Med. 1980, 302, 1128–1131. [Google Scholar] [CrossRef] [PubMed]
- Garbinski, L.D.; Rosen, B.P.; Chen, J. Pathways of arsenic uptake and efflux. Environ. Int. 2019, 126, 585–597. [Google Scholar] [CrossRef] [PubMed]
- Zhao, J.; Li, A.; Mei, Y.; Zhou, Q.; Li, Y.; Li, K.; Xu, Q. The association of arsenic exposure with hypertension and blood pressure: A systematic review and dose-response meta-analysis. Environ. Pollut. 2021, 289, 117914. [Google Scholar] [CrossRef]
- Oremland, R.S.; Stolz, J.F. The ecology of arsenic. Science 2003, 300, 939–944. [Google Scholar] [CrossRef] [PubMed]
- Kumagai, T.; Shih, L.Y.; Hughes, S.V.; Desmond, J.C.; O’Kelly, J.; Hewison, M.; Koeffler, H.P. 19-Nor-1,25(OH)2D2 (a novel, noncalcemic vitamin D analogue), combined with arsenic trioxide, has potent antitumor activity against myeloid leukemia. Cancer Res. 2005, 65, 2488–2497. [Google Scholar] [CrossRef]
- Zamoiski, R.D.; Guallar, E.; García-Vargas, G.G.; Rothenberg, S.J.; Resnick, C.; Andrade, M.R.; Steuerwald, A.J.; Parsons, P.J.; Weaver, V.M.; Navas-Acien, A.; et al. Association of arsenic and metals with concentrations of 25-hydroxyvitamin D and 1,25-dihydroxyvitamin D among adolescents in Torreón, Mexico. Environ. Health Perspect. 2014, 122, 1233–1238. [Google Scholar] [CrossRef]
- Fang, X.; Qu, J.; Huan, S.; Sun, X.; Li, J.; Liu, Q.; Jin, S.; Xia, W.; Xu, S.; Wu, Y.; et al. Associations of urine metals and metal mixtures during pregnancy with cord serum vitamin D Levels: A prospective cohort study with repeated measurements of maternal urinary metal concentrations. Environ. Int. 2021, 155, 106660. [Google Scholar] [CrossRef]
- Ameer, S.S.; Xu, Y.; Engström, K.; Li, H.; Tallving, P.; Nermell, B.; Boemo, A.; Parada, L.A.; Peñaloza, L.G.; Concha, G.; et al. Exposure to Inorganic Arsenic Is Associated with Increased Mitochondrial DNA Copy Number and Longer Telomere Length in Peripheral Blood. Front. Cell Dev. Biol. 2016, 4, 87. [Google Scholar] [CrossRef]
- Ventura-Lima, J.; Bogo, M.R.; Monserrat, J.M. Arsenic toxicity in mammals and aquatic animals: A comparative biochemical approach. Ecotoxicol. Environ. Saf. 2011, 74, 211–218. [Google Scholar] [CrossRef]
- Mandal, B.K.; Ogra, Y.; Suzuki, K.T. Identification of dimethylarsinous and monomethylarsonous acids in human urine of the arsenic-affected areas in West Bengal, India. Chem. Res. Toxicol. 2001, 14, 371–378. [Google Scholar] [CrossRef]
- Le, X.C.; Lu, X.; Ma, M.; Cullen, W.R.; Aposhian, H.V.; Zheng, B. Speciation of key arsenic metabolic intermediates in human urine. Anal. Chem. 2000, 72, 5172–5177. [Google Scholar] [CrossRef]
- Hopenhayn-Rich, C.; Biggs, M.L.; Smith, A.H.; Kalman, D.A.; Moore, L.E. Methylation study of a population environmentally exposed to arsenic in drinking water. Environ. Health Perspect. 1996, 104, 620–628. [Google Scholar] [CrossRef] [PubMed]
- Gong, Z.; Lu, X.; Cullen, W.R.; Le, X.C.J.J.o.A.A.S. Unstable trivalent arsenic metabolites, monomethylarsonous acid and dimethylarsinous acid. J. Anal. At. Spectrom. 2001, 16, 1409–1413. [Google Scholar] [CrossRef]
- Gardner, R.M.; Nermell, B.; Kippler, M.; Grandér, M.; Li, L.; Ekström, E.C.; Rahman, A.; Lönnerdal, B.; Hoque, A.M.; Vahter, M. Arsenic methylation efficiency increases during the first trimester of pregnancy independent of folate status. Reprod. Toxicol. 2011, 31, 210–218. [Google Scholar] [CrossRef]
- Vahter, M.E. Interactions between arsenic-induced toxicity and nutrition in early life. J. Nutr. 2007, 137, 2798–2804. [Google Scholar] [CrossRef] [PubMed]
- De Loma, J.; Tirado, N.; Ascui, F.; Levi, M.; Vahter, M.; Broberg, K.; Gardon, J. Elevated arsenic exposure and efficient arsenic metabolism in indigenous women around Lake Poopó, Bolivia. Sci. Total Environ. 2019, 657, 179–186. [Google Scholar] [CrossRef]
- Olmos, V.; Astolfo, M.A.; Sassone, A.H.; Villaamil Lepori, E.C. The level of exposure affects the arsenic urinary methylation profile of a population of children. J. Hazard. Mater. 2021, 415, 125623. [Google Scholar] [CrossRef]
- Bikle, D.D. Vitamin D metabolism and function in the skin. Mol. Cell. Endocrinol. 2011, 347, 80–89. [Google Scholar] [CrossRef]
- DeLuca, H.F. Overview of general physiologic features and functions of vitamin D. Am. J. Clin. Nutr. 2004, 80, 1689s–1696s. [Google Scholar] [CrossRef]
- Chen, T.C.; Chimeh, F.; Lu, Z.; Mathieu, J.; Person, K.S.; Zhang, A.; Kohn, N.; Martinello, S.; Berkowitz, R.; Holick, M.F. Factors that influence the cutaneous synthesis and dietary sources of vitamin D. Arch. Biochem. Biophys. 2007, 460, 213–217. [Google Scholar] [CrossRef]
- Yu, H.S.; Liao, W.T.; Chai, C.Y. Arsenic carcinogenesis in the skin. J. Biomed. Sci. 2006, 13, 657–666. [Google Scholar] [CrossRef]
- Kennel, K.A.; Drake, M.T.; Hurley, D.L. Vitamin D deficiency in adults: When to test and how to treat. Mayo Clin. Proc. 2010, 85, 752–757. [Google Scholar] [CrossRef]
- Wiciński, M.; Adamkiewicz, D.; Adamkiewicz, M.; Śniegocki, M.; Podhorecka, M.; Szychta, P.; Malinowski, B. Impact of Vitamin D on Physical Efficiency and Exercise Performance—A Review. Nutrients 2019, 11, 2826. [Google Scholar] [CrossRef]
- Mazur, A.; Koziorowska, K.; Dynarowicz, K.; Aebisher, D.; Bartusik-Aebisher, D. Vitamin D and Vitamin D3 Supplementation during Photodynamic Therapy: A Review. Nutrients 2022, 14, 3805. [Google Scholar] [CrossRef]
- Jäpelt, R.B.; Jakobsen, J. Vitamin D in plants: A review of occurrence, analysis, and biosynthesis. Front. Plant Sci. 2013, 4, 136. [Google Scholar] [CrossRef]
- Cashman, K.D.; Kiely, M. EURRECA-Estimating vitamin D requirements for deriving dietary reference values. Crit. Rev. Food Sci. Nutr. 2013, 53, 1097–1109. [Google Scholar] [CrossRef]
- Castano, L.; Madariaga, L.; Grau, G.; García-Castaño, A. 25(OH)Vitamin D Deficiency and Calcifediol Treatment in Pediatrics. Nutrients 2022, 14, 1854. [Google Scholar] [CrossRef]
- Pei, K.L.; Gailer, J. Probing the interaction of arsenobetaine with blood plasma constituents in vitro: An SEC-ICP-AES study. Met. Integr. Biometal. Sci. 2009, 1, 403–408. [Google Scholar] [CrossRef]
- Chen, H.; Zhang, H.; Wang, X.; Wu, Y.; Zhang, Y.; Chen, S.; Zhang, W.; Sun, X.; Zheng, T.; Xia, W.; et al. Prenatal arsenic exposure, arsenic metabolism and neurocognitive development of 2-year-old children in low-arsenic areas. Environ. Int. 2023, 174, 107918. [Google Scholar] [CrossRef]
- Tseng, C.H. A review on environmental factors regulating arsenic methylation in humans. Toxicol. Appl. Pharmacol. 2009, 235, 338–350. [Google Scholar] [CrossRef]
- Pierce, B.L.; Tong, L.; Argos, M.; Gao, J.; Farzana, J.; Roy, S.; Paul-Brutus, R.; Rahaman, R.; Rakibuz-Zaman, M.; Parvez, F.; et al. Arsenic metabolism efficiency has a causal role in arsenic toxicity: Mendelian randomization and gene-environment interaction. Int. J. Epidemiol. 2013, 42, 1862–1871. [Google Scholar] [CrossRef] [PubMed]
- Valenzuela, O.L.; Borja-Aburto, V.H.; Garcia-Vargas, G.G.; Cruz-Gonzalez, M.B.; Garcia-Montalvo, E.A.; Calderon-Aranda, E.S.; Del Razo, L.M. Urinary trivalent methylated arsenic species in a population chronically exposed to inorganic arsenic. Environ. Health Perspect. 2005, 113, 250–254. [Google Scholar] [CrossRef]
- Bangert, C.; Brunner, P.M.; Stingl, G. Immune functions of the skin. Clin. Dermatol. 2011, 29, 360–376. [Google Scholar] [CrossRef]
- Wu, S.; Zhao, M.; Sun, Y.; Xie, M.; Le, K.; Xu, M.; Huang, C. The potential of Diosgenin in treating psoriasis: Studies from HaCaT keratinocytes and imiquimod-induced murine model. Life Sci. 2020, 241, 117115. [Google Scholar] [CrossRef] [PubMed]
- Lehmann, B.; Genehr, T.; Knuschke, P.; Pietzsch, J.; Meurer, M. UVB-induced conversion of 7-dehydrocholesterol to 1alpha,25-dihydroxyvitamin D3 in an in vitro human skin equivalent model. J. Investig. Dermatol. 2001, 117, 1179–1185. [Google Scholar] [CrossRef]
- Bikle, D.D.; Nemanic, M.K.; Gee, E.; Elias, P. 1,25-Dihydroxyvitamin D3 production by human keratinocytes. Kinetics and regulation. J. Clin. Investig. 1986, 78, 557–566. [Google Scholar] [CrossRef] [PubMed]
- Gailer, J.; Madden, S.; Cullen, W.R.; Denton, M.B. The separation of dimethylarsinic acid, methylarsonous acid, methylarsonic acid, arsenate and dimethylarsinous acid on the Hamilton PRP-X100 anion-exchange column. Appl. Organomet. Chem. 1999, 13, 837–843. [Google Scholar] [CrossRef]
Characteristics | Value |
---|---|
Age, years, mean ± SD | 57.92 ± 10.80 |
BMI, kg/m2, mean ± SD | 25.77 ± 4.01 |
Gender, n (%) | |
Male | 256 (33.7) |
Female | 506 (66.3) |
Skin hyperkeratosis | |
No | 495 (64.9) |
Yes | 267 (35.1) |
Occupation, n (%) | |
Farmer | 657 (86.1) |
Others | 105 (13.9) |
Education, n (%) | |
Primary and below | 269 (35.4) |
Junior high school | 409 (53.6) |
Senior high school and above | 84 (11) |
Milk consumption, n (%) | |
≤1/week | 471 (61.8) |
>1/week | 291 (38.2) |
Urinary tAs, μg/L, median (P25–P75) | 69.81 (27.77–137.51) |
Urinary iAs, μg/L, median (P25–P75) | 3.46 (0.83–14.67) |
Urinary MMAV, μg/L, median (P25–P75) | 4.78 (0.32–16.14) |
Urinary DMAV, μg/L, median (P25–P75) | 51.15 (19.00–102.93) |
Urinary iAs%, median (P25–P75) | 9.94 (2.39–18.58) |
Urinary MMAV%, median (P25–P75) | 9.41 (1.60–16.88) |
Urinary DMAV%, median (P25–P75) | 78.48 (66.53–90.18) |
PMI, median (P25–P75) | 89.81 (81.26–97.51) |
SMI, median (P25–P75) | 89.15 (80.02–97.93) |
Blood glucose, mmol/L, median (P25–P75) | 5.70 (5.10–6.70) |
25(OH)D, ng/mL, mean ± SD | 74.03 ± 22.67 |
Exposure | Box–Cox Transformed β (95% CI) | p-Value |
---|---|---|
tAs | ||
Model 1 | 0.046 (0.020, 0.071) | <0.01 |
Model 2 | 0.044 (0.021, 0.067) | <0.01 |
Model 3 | 0.044 (0.020, 0.069) | <0.01 |
iAs | ||
Model 1 | 0.330 (0.035, 0.624) | 0.028 |
Model 2 | 0.155 (−0.115, 0.425) | 0.260 |
Model 3 | 0.100 (−0.178, 0.377) | 0.482 |
MMAV | ||
Model 1 | 0.447 (0.145, 0.748) | <0.01 |
Model 2 | 0.276 (0.001, 0.551) | 0.049 |
Model 3 | 0.272 (−0.013, 0.556) | 0.061 |
DMAV | ||
Model 1 | 0.057 (0.024, 0.089) | <0.01 |
Model 2 | 0.060 (0.031, 0.091) | <0.01 |
Model 3 | 0.062 (0.030, 0.094) | <0.01 |
Exposure | Box–Cox Transformed β | Box–Cox Transformed RR (95% CI) | p-Value |
---|---|---|---|
tAs | |||
Model 1 | 0.004 | 1.004 (1.001, 1.006) | 0.016 |
Model 2 | 0.003 | 1.003 (1.000, 1.005) | 0.079 |
iAs | |||
Model 1 | 0.020 | 1.020 (0.987, 1.054) | 0.240 |
Model 2 | 0.002 | 1.002 (0.974, 1.302) | 0.869 |
MMAV | |||
Model 1 | 0.022 | 1.022 (0.988, 1.057) | 0.200 |
Model 2 | 0.004 | 1.004 (0.973, 1.037) | 0.784 |
DMAV | |||
Model 1 | 0.005 | 1.005 (1.001, 1.008) | 0.011 |
Model 2 | 0.004 | 1.004 (1.000, 1.008) | 0.030 |
Box–Cox Transformed β (95% CI) b | p-Value b | |
---|---|---|
iAs% a | ||
<10.19 | 0.015 (−0.027, 0.057) | 0.484 |
≥10.19 | 0.064 (0.032, 0.096) | <0.01 |
MMAV% a | ||
<9.54 | 0.053 (0.012, 0.094) | 0.036 |
≥9.54 | 0.038 (0.006, 0.070) | 0.044 |
DMAV% a | ||
<78.15 | 0.046 (0.013, 0.078) | <0.01 |
≥78.15 | 0.047 (0.006, 0.087) | 0.027 |
PMI | ||
<89.81 | 0.064 (0.032, 0.096) | <0.01 |
≥89.81 | 0.015 (−0.027, 0.057) | 0.484 |
SMI | ||
<89.15 | 0.041 (0.009, 0.073) | 0.013 |
≥89.15 | 0.050 (0.009, 0.091) | 0.017 |
Box–Cox Transformed β (95% CI) a | ||||
---|---|---|---|---|
Exposure | Normal | p-Value | Skin Hyperkeratosis | p-Value |
tAs | 0.041 (0.013, 0.069) | <0.01 | 0.046 (−0.007, 0.099) | 0.090 |
iAs | 0.169 (−0.173, 0.511) | 0.332 | 0.592 (0.041, 1.143) | 0.035 |
MMAV | 0.425 (0.075, 0.776) | <0.01 | 0.430 (−0.139, 0.999) | 0.138 |
DMAV | 0.054 (0.017, 0.090) | <0.01 | 0.052 (−0.015, 0.119) | 0.129 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, K.; Yin, Y.; Lv, M.; Zhang, X.; Zhang, M.; Cui, J.; Guan, Z.; Liu, X.; Liu, Y.; Gao, Y.; et al. Positive Association of Urinary Dimethylarsinic Acid (DMAV) with Serum 25(OH)D in Adults Living in an Area of Water-Borne Arsenicosis in Shanxi, China. Toxics 2024, 12, 83. https://doi.org/10.3390/toxics12010083
Zhang K, Yin Y, Lv M, Zhang X, Zhang M, Cui J, Guan Z, Liu X, Liu Y, Gao Y, et al. Positive Association of Urinary Dimethylarsinic Acid (DMAV) with Serum 25(OH)D in Adults Living in an Area of Water-Borne Arsenicosis in Shanxi, China. Toxics. 2024; 12(1):83. https://doi.org/10.3390/toxics12010083
Chicago/Turabian StyleZhang, Kunyu, Yunyi Yin, Man Lv, Xin Zhang, Meichen Zhang, Jia Cui, Ziqiao Guan, Xiaona Liu, Yang Liu, Yanhui Gao, and et al. 2024. "Positive Association of Urinary Dimethylarsinic Acid (DMAV) with Serum 25(OH)D in Adults Living in an Area of Water-Borne Arsenicosis in Shanxi, China" Toxics 12, no. 1: 83. https://doi.org/10.3390/toxics12010083