Abstract
Celiac disease (CD) is an autoimmune disease with increasing prevalence in the USA. CD leads to decreased absorption of many nutrients including certain divalent metals. On the other hand, recent cross-sectional studies suggest the associations between trace heavy metal exposure and autoimmunity. We aimed to determine if there is an association between CD autoimmunity and blood levels of heavy metals in the general US population. We used nationally representative data from National Health and Nutrition Examination Survey, 2009–2012. Our study comprised 3643 children (ages 6–17 years) and 11,040 adults (age ≥18 years). Children with CD seropositivity had significantly lower blood lead (0.56 versus 0.80 μg/dL, P = 0.001) and mercury levels (0.47 versus 0.64 μg/L, P = 0.001). In the linear regression model, CD seropositivity was associated with lower levels of blood lead and mercury in children (β = −0.14, P = 0.03 for lead and β = −0.22, P = 0.008 for mercury), but not in adults. These findings of CD-heavy metals association are, to our knowledge, novel, and we conclude that decreased levels of heavy metals in blood are most likely a consequence of CD in the US children.
Similar content being viewed by others
References
Berk M, Williams LJ, Andreazza AC, Pasco JA, Dodd S, Jacka FN, Moylan S, Reiner EJ, Magalhaes PV (2014) Pop, heavy metal and the blues: secondary analysis of persistent organic pollutants (POP), heavy metals and depressive symptoms in the NHANES National Epidemiological Survey. BMJ Open 4:e005142
Breton J, Daniel C, Dewulf J, Pothion S, Froux N, Sauty M, Thomas P, Pot B, Foligne B (2013) Gut microbiota limits heavy metals burden caused by chronic oral exposure. Toxicol Lett 222:132–138
Caruso R, Pallone F, Stasi E, Romeo S, Monteleone G (2013) Appropriate nutrient supplementation in celiac disease. Ann Med 45:522–531
Clarkson TW, Magos L, Myers GJ (2003) The toxicology of mercury—current exposures and clinical manifestations. N Engl J Med 349:1731–1737
Cojocaru M, Chicos B (2014) The role of heavy metals in autoimmunity. Romanian Journal of Internal Medicine = Revue Roumaine de Medecine Interne 52:189–191
deSilva PE (1984) Blood lead levels and the haematocrit correction. The Annals of Occupational Hygiene 28:417–428
Dietert RR, Zelikoff JT (2010) Identifying patterns of immune-related disease: use in disease prevention and management. World Journal of Pediatrics : WJP 6:111–118
Dyer AA, Rivkina V, Perumal D, Smeltzer BM, Smith BM, Gupta RS (2015) Epidemiology of childhood peanut allergy. Allergy and Asthma Proceedings 36:58–64
Elli L, Rossi V, Conte D, Ronchi A, Tomba C, Passoni M, Bardella MT, Roncoroni L, Guzzi G (2015) Increased mercury levels in patients with celiac disease following a gluten-free regimen. Gastroenterol Res Pract 2015:953042
Freeman HJ (2015) Iron deficiency anemia in celiac disease. World J Gastroenterol 21:9233–9238
Hannaway PJ, Connelly ME, Cobbett RM, Dobrow PJ (2005) Differences in race, ethnicity, and socioeconomic status in schoolchildren dispensed injectable epinephrine in 3 Massachusetts school districts. Annals of Allergy, Asthma & Immunology: Official Publication of the American College of Allergy, Asthma, & Immunology 95:143–148
Janicka M, Binkowski LJ, Blaszczyk M, Paluch J, Wojtas W, Massanyi P, Stawarz R (2015) Cadmium, lead and mercury concentrations and their influence on morphological parameters in blood donors from different age groups from southern Poland. Journal of Trace Elements in Medicine and Biology: Organ of the Society for Minerals and Trace Elements 29:342–346
Jansson SA, Protudjer JL, Arnlind Heibert M, Bengtsson U, Kallstrom-Bengtsson I, Marklund B, Middelveld RJ, Rentzos G, Sundqvist AC, Akerstrom J, Ostblom E, Dahlen SE, Ahlstedt S (2014) Socioeconomic evaluation of well-characterized allergy to staple foods in adults. Allergy 69:1241–1247
Kahn LG, Liu X, Rajovic B, Popovac D, Oberfield S, Graziano JH, Factor-Litvak P (2014) Blood lead concentration and thyroid function during pregnancy: results from the Yugoslavia Prospective Study of Environmental Lead Exposure. Environ Health Perspect 122:1134–1140
Khalid AN, McMains KC (2016) Gluten sensitivity: fact or fashion statement? Current Opinion in Otolaryngology & Head and Neck Surgery 24:238–240
Kim BM, Choi AL, Ha EH, Pedersen L, Nielsen F, Weihe P, Hong YC, Budtz-Jorgensen E, Grandjean P (2014) Effect of hemoglobin adjustment on the precision of mercury concentrations in maternal and cord blood. Environ Res 132:407–412
Leonard MM, Camhi S, Huedo-Medina TB, Fasano A (2015) Celiac Disease Genomic, Environmental, Microbiome, and Metabolomic (CDGEMM) Study Design: approach to the future of personalized prevention of celiac disease. Nutrients 7:9325–9336
Lepow ML, Bruckman L, Gillette M, Markowitz S, Robino R, Kapish J (1975) Investigations into sources of lead in the environment of urban children. Environ Res 10:415–426
Ludvigsson JF et al (2014) Diagnosis and management of adult coeliac disease: guidelines from the British Society of Gastroenterology. Gut 63:1210–1228
Lundh T, Axmon A, Skerfving S, Broberg K (2016) Cadmium and mercury exposure over time in Swedish children. Environ Res 150:600–605
Marasco G, Di Biase AR, Schiumerini R, Eusebi LH, Iughetti L, Ravaioli F, Scaioli E, Colecchia A, Festi D (2016) Gut microbiota and celiac disease. Dig Dis Sci 61:1461–1472
Mardini HE, Westgate P, Grigorian AY (2015) Racial differences in the prevalence of celiac disease in the US population: National Health and Nutrition Examination Survey (NHANES) 2009-2012. Dig Dis Sci 60:1738–1742
Morales ME, Derbes RS, Ade CM, Ortego JC, Stark J, Deininger PL, Roy-Engel AM (2016) Heavy metal exposure influences double strand break DNA repair outcomes. PLoS One 11:e0151367
Mostafa GA, Bjorklund G, Urbina MA, Al-Ayadhi LY (2016) The levels of blood mercury and inflammatory-related neuropeptides in the serum are correlated in children with autism spectrum disorder. Metab Brain Dis 31:593–599
Nielsen SJ, Kit BK, Aoki Y, Ogden CL (2014) Seafood consumption and blood mercury concentrations in adults aged ≥20 y, 2007-2010. Am J Clin Nutr 99:1066–1070
Nielsen SJ, Aoki Y, Kit BK, Ogden CL (2015) More than half of US youth consume seafood and most have blood mercury concentrations below the EPA reference level, 2009-2012. J Nutr 145:322–327
Pirkle JL, Brody DJ, Gunter EW, Kramer RA, Paschal DC, Flegal KM, Matte TD (1994) The decline in blood lead levels in the United States. The National Health and Nutrition Examination Surveys (NHANES). JAMA 272:284–291
Rubio-Tapia A, Ludvigsson JF, Brantner TL, Murray JA, Everhart JE (2012) The prevalence of celiac disease in the United States. Am J Gastroenterol 107:1538–1544 quiz 1537, 1545
Singh VK, Mishra KP, Rani R, Yadav VS, Awasthi SK, Garg SK (2003) Immunomodulation by lead. Immunol Res 28:151–166
Theethira TG, Dennis M, Leffler DA (2014) Nutritional consequences of celiac disease and the gluten-free diet. Expert Review of Gastroenterology & Hepatology 8:123–129
Wu J, Wen XW, Faulk C, Boehnke K, Zhang H, Dolinoy DC, Xi C (2016a) Perinatal lead exposure alters gut microbiota composition and results in sex-specific bodyweight increases in adult mice. Toxicological Sciences: an Official Journal of the Society of Toxicology 151:324–333
Wu X, Cobbina SJ, Mao G, Xu H, Zhang Z, Yang L (2016b) A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ Sci Pollut Res Int 23:8244–8259
Yeter D, Portman MA, Aschner M, Farina M, Chan WC, Hsieh KS, Kuo HC (2016): Ethnic Kawasaki disease risk associated with blood mercury and cadmium in U.S. children. Int J Environ Res Public Health 13:1–14
Acknowledgements
Elena Kamycheva has received the financial support from the Medical Clinic, University Hospital of North Norway, Sykehusveien 38, 9038 Tromsoe, Norway.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Source of funding
E.K. received financial support from the Medical Clinic, University Hospital of North Norway, Tromsoe, Norway.
Conflicts of interest
The authors declare that they have no conflicts of interest.
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Kamycheva, E., Goto, T. & Camargo, C.A. Blood levels of lead and mercury and celiac disease seropositivity: the US National Health and Nutrition Examination Survey. Environ Sci Pollut Res 24, 8385–8391 (2017). https://doi.org/10.1007/s11356-017-8545-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-8545-0