PCBs and Dioxins Either Cause or Make Worse Both Osteo and Rheumatoid Arthritis
Main Article Content
Abstract
Rheumatoid arthritis is an autoimmune disease, while osteoarthritis is presumed to be a disease due to wear and tear causing damage to joints. Some environmental exposures, such as smoking, air pollution and possibly persistent organic pollutants, are known to increase the risk of both. We have utilized the National Health and Nutrition Examination Survey (NHANES) data to determine associations between self-reported prevalence of any form of arthritis, rheumatoid and osteoarthritis and various polychlorinated biphenyl (PCB) congeners, several chlorinated pesticides and 2.3,7,8-tetrachloro-dibenzo-dioxin (TCDD). We find that there is a statistically significant association between serum PCB levels of more highly chlorinated PCB congeners and both types of arthritis. The associations are stronger with rheumatoid arthritis than with osteoarthritis, and stronger in women than in men.
Keywords:
Rheumatoid arthritis, Osteo-arthritis, NHANES, Persistent organic pollutants, Polychlorinated biphenyls, Chlorinated pesticides
Article Details
How to Cite
MOHAMMAD, Azad; CARPENTER, David O..
PCBs and Dioxins Either Cause or Make Worse Both Osteo and Rheumatoid Arthritis.
Medical Research Archives, [S.l.], v. 10, n. 7, july 2022.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2900>. Date accessed: 22 dec. 2024.
doi: https://doi.org/10.18103/mra.v10i7.2900.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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11. Stolt P, Bengtsson C, Nordmark B, et al. Quantification of the influence of cigarette smoking on rheumatoid arthritis: results from a population based case-control study, using incident cases. Ann Rheum Dis. 2003;62(9):835-841. doi:10.1136/ard.62.9.835
12. Farhat SC, Silva CA, Orione MA, Campos LM, Sallum AM, Braga AL. Air pollution in autoimmune rheumatic diseases: a review. Autoimmun Rev. 2011;11(1):14-21. doi:10.1016/j.autrev.2011.06.008
13. Hart JE, Laden F, Puett RC, Costenbader KH, Karlson EW. Exposure to traffic pollution and increased risk of rheumatoid arthritis. Environ Health Perspect. 2009;117(7):1065-1069. doi:10.1289/ehp.0800503
14. Gan RW, Deane KD, Zerbe GO, et al. Relationship between air pollution and positivity of RA-related autoantibodies in individuals without established RA: a report on SERA. Ann Rheum Dis. 2013;72(12):2002-2005. doi:10.1136/annrheumdis-2012-202949
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17. Carpenter DO. Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health. Rev Environ Health. 2006;21(1):1-23. doi:10.1515/reveh.2006.21.1.1
18. Lan SJ, Yen YY, Lan JL, Chen ER, Ko YC. Immunity of PCB transplacental Yu-Cheng children in Taiwan. Bull Environ Contam Toxicol. 1990;44(2):224-229. doi:10.1007/BF01700140
19. Guo, Y. L. L., Yu, M. L., Hsu, C. C., & Rogan, W. J. (1999). Chloracne, goiter, arthritis, and anemia after polychlorinated biphenyl poisoning: 14-year follow-up of the Taiwan Yucheng cohort. Environmental Health Perspectives, 107(9), 715-719. doi:Doi 10.2307/3434656
20. Abella V, Santoro A, Scotece M, et al. Non-dioxin-like polychlorinated biphenyls (PCB 101, PCB 153 and PCB 180) induce chondrocyte cell death through multiple pathways. Toxicol Lett. 2015;234(1):13-19. doi:10.1016/j.toxlet.2015.02.001
21. Lee HG, Yang JH. PCB126 induces apoptosis of chondrocytes via ROS-dependent pathways. Osteoarthritis Cartilage. 2012;20(10):1179-1185. doi:10.1016/j.joca.2012.06.004
22. Kobayashi S, Okamoto H, Iwamoto T, et al. A role for the aryl hydrocarbon receptor and the dioxin TCDD in rheumatoid arthritis. Rheumatology (Oxford). 2008;47(9):1317-1322. doi:10.1093/rheumatology/ken259
23. Lee DH, Steffes M, Jacobs DR. Positive associations of serum concentration of polychlorinated biphenyls or organochlorine pesticides with self-reported arthritis, especially rheumatoid type, in women. Environ Health Perspect. 2007;115(6):883-888. doi:10.1289/ehp.9887
24. Turner W., DiPietro E., Lapeza C., Green V., Gill J., Patterson, D.G. , Jr. A fast universal automated cleanup system for the isotope-dilution highresolution mass spectrometric analysis of pcdds, pcdfs, coplanar pcbs, pcb congeners, and persistent pesticides from the same serum sample. Organohalogen compounds 31: 26-31 (1997).
25. Patterson DG Jr, Wong LY, Turner WE, et al. Levels in the U.S. population of those persistent organic pollutants (2003-2004) included in the Stockholm Convention or in other long range transboundary air pollution agreements. Environ Sci Technol. 2009;43(4):1211-1218. doi:10.1021/es801966w
26. Carpenter DO. Exposure to and health effects of volatile PCBs. Rev Environ Health. 2015;30(2):81-92. doi:10.1515/reveh-2014-0074
27. ATSDR, Thallium. "ATSDR (Agency for toxic substances and disease registry)." Prepared by clement international corp., under contract 205 (2000): 88-0608.
28. Kanagawa Y, Matsumoto S, Koike S, et al. Association of clinical findings in Yusho patients with serum concentrations of polychlorinated biphenyls, polychlorinated quarterphenyls and 2,3,4,7,8-pentachlorodibenzofuran more than 30 years after the poisoning event. Environ Health. 2008;7:47. Published 2008 Oct 2. doi:10.1186/1476-069X-7-47
29. Guo YL, Yu ML, Hsu CC, Rogan WJ. Chloracne, goiter, arthritis, and anemia after polychlorinated biphenyl poisoning: 14-year follow-Up of the Taiwan Yucheng cohort. Environ Health Perspect. 1999;107(9):715-719. doi:10.1289/ehp.99107715
30. Li MC, Tsai PC, Chen PC, Hsieh CJ, Leon Guo YL, Rogan WJ. Mortality after exposure to polychlorinated biphenyls and dibenzofurans: 30 years after the "Yucheng accident". Environ Res. 2013;120:71-75. doi:10.1016/j.envres.2012.09.003
31. Azamar-Llamas D, Hernández-Molina G, Ramos-Ávalos B, Furuzawa-Carballeda J. Adipokine contribution to the pathogenesis of osteoarthritis. Mediators Inflamm. 2017;2017:5468023. doi:10.1155/2017/5468023
32. Valentine, R. J., Vieira, V. J., Woods, J. A., & Evans, E. M. (2009). Stronger relationship between central adiposity and C-reactive protein in older women than men. Menopause, 16(1), 84-89
33. Khera A, McGuire DK, Murphy SA, et al. Race and gender differences in C-reactive protein levels. J Am Coll Cardiol. 2005;46(3):464-469. doi:10.1016/j.jacc.2005.04.051
34. Giles JT, Bartlett SJ, Andersen R, Thompson R, Fontaine KR, Bathon JM. Association of body fat with C-reactive protein in rheumatoid arthritis. Arthritis Rheum. 2008;58(9):2632-2641. doi:10.1002/art.23766.
35. Tabb MM, Kholodovych V, Grün F, Zhou C, Welsh WJ, Blumberg B. Highly chlorinated PCBs inhibit the human xenobiotic response mediated by the steroid and xenobiotic receptor (SXR). Environ Health Perspect. 2004;112(2):163-169. doi:10.1289/ehp.6560
36. Al-Salman F, Plant N. Non-coplanar polychlorinated biphenyls (PCBs) are direct agonists for the human pregnane-X receptor and constitutive androstane receptor, and activate target gene expression in a tissue-specific manner. Toxicol Appl Pharmacol. 2012;263(1):7-13. doi:10.1016/j.taap.2012.05.016
37. Kamata R, Shiraishi F, Kageyama S, Nakajima D. Detection and measurement of the agonistic activities of PCBs and mono-hydroxylated PCBs to the constitutive androstane receptor using a recombinant yeast assay. Toxicol In Vitro. 2015;29(7):1859-1867. doi:10.1016/j.tiv.2015.07.021
38. Kamata R, Nakajima D, Shiraishi F. Measurement of the agonistic activities of monohydroxylated polychlorinated biphenyls at the retinoid X and retinoic acid receptors using recombinant yeast cells. Toxicol In Vitro. 2019;57:9-17. doi:10.1016/j.tiv.2019.01.022
39. Johnson CD, Balagurunathan Y, Tadesse MG, et al. Unraveling gene-gene interactions regulated by ligands of the aryl hydrocarbon receptor. Environ Health Perspect. 2004;112(4):403-412. doi:10.1289/ehp.6758
40. Maier MS, Legare ME, Hanneman WH. The aryl hydrocarbon receptor agonist 3,3',4,4',5-pentachlorobiphenyl induces distinct patterns of gene expression between hepatoma and glioma cells: chromatin remodeling as a mechanism for selective effects. Neurotoxicology. 2007;28(3):594-612.
2. Cross M, Smith E, Hoy D, et al. The global burden of hip and knee osteoarthritis: estimates from the global burden of disease 2010 study. Ann Rheum Dis. 2014;73(7):1323-1330. doi:10.1136/annrheumdis-2013-204763
3. GBD 2013 DALYs and HALE Collaborators, Murray CJ, Barber RM, et al. Global, regional, and national disability-adjusted life years (DALYs) for 306 diseases and injuries and healthy life expectancy (HALE) for 188 countries, 1990-2013: quantifying the epidemiological transition. Lancet. 2015;386(10009):2145-2191. doi:10.1016/S0140-6736(15)61340-X
4. Guo Q, Wang Y, Xu D, Nossent J, Pavlos NJ, Xu J. Rheumatoid arthritis: pathological mechanisms and modern pharmacologic therapies. Bone Res. 2018;6:15. Published 2018 Apr 27. doi:10.1038/s41413-018-0016-9
5. Medina G, Vera-Lastra O, Peralta-Amaro AL, et al. Metabolic syndrome, autoimmunity and rheumatic diseases. Pharmacol Res. 2018;133:277-288. doi:10.1016/j.phrs.2018.01.009
6. Hartz AJ, Fischer ME, Bril G, et al. The association of obesity with joint pain and osteoarthritis in the NHANES data. J Chronic Dis. 1986;39(4):311-319. doi:10.1016/0021-9681(86)90053-6
7. Gremese E, Tolusso B, Gigante MR, Ferraccioli G. Obesity as a risk and severity factor in rheumatic diseases (autoimmune chronic inflammatory diseases). Front Immunol. 2014;5:576. Published 2014 Nov 11. doi:10.3389/fimmu.2014.00576
8. Mohammed A, Alshamarri T, Adeyeye T, Lazariu V, McNutt LA, Carpenter DO. A comparison of risk factors for osteo- and rheumatoid arthritis using NHANES data. Prev Med Rep. 2020;20:101242. Published 2020 Nov 5. doi:10.1016/j.pmedr.2020.101242.
9. MacDonald IJ, Liu SC, Huang CC, Kuo SJ, Tsai CH, Tang CH. Associations between adipokines in arthritic disease and implications for obesity. Int J Mol Sci. 2019;20(6):1505. Published 2019 Mar 26. doi:10.3390/ijms20061505
10. Haugen IK, Magnusson K, Turkiewicz A, Englund M. The prevalence, incidence, and progression of hand osteoarthritis in relation to body mass index, smoking, and alcohol consumption. J Rheumatol. 2017;44(9):1402-1409. doi:10.3899/jrheum.170026
11. Stolt P, Bengtsson C, Nordmark B, et al. Quantification of the influence of cigarette smoking on rheumatoid arthritis: results from a population based case-control study, using incident cases. Ann Rheum Dis. 2003;62(9):835-841. doi:10.1136/ard.62.9.835
12. Farhat SC, Silva CA, Orione MA, Campos LM, Sallum AM, Braga AL. Air pollution in autoimmune rheumatic diseases: a review. Autoimmun Rev. 2011;11(1):14-21. doi:10.1016/j.autrev.2011.06.008
13. Hart JE, Laden F, Puett RC, Costenbader KH, Karlson EW. Exposure to traffic pollution and increased risk of rheumatoid arthritis. Environ Health Perspect. 2009;117(7):1065-1069. doi:10.1289/ehp.0800503
14. Gan RW, Deane KD, Zerbe GO, et al. Relationship between air pollution and positivity of RA-related autoantibodies in individuals without established RA: a report on SERA. Ann Rheum Dis. 2013;72(12):2002-2005. doi:10.1136/annrheumdis-2012-202949
15. De Roos AJ, Koehoorn M, Tamburic L, Davies HW, Brauer M. Proximity to traffic, ambient air pollution, and community noise in relation to incident rheumatoid arthritis. Environ Health Perspect. 2014;122(10):1075-1080. doi:10.1289/ehp.1307413
16. Hart JE, Källberg H, Laden F, et al. Ambient air pollution exposures and risk of rheumatoid arthritis. Arthritis Care Res (Hoboken). 2013;65(7):1190-1196. doi:10.1002/acr.21975
17. Carpenter DO. Polychlorinated biphenyls (PCBs): routes of exposure and effects on human health. Rev Environ Health. 2006;21(1):1-23. doi:10.1515/reveh.2006.21.1.1
18. Lan SJ, Yen YY, Lan JL, Chen ER, Ko YC. Immunity of PCB transplacental Yu-Cheng children in Taiwan. Bull Environ Contam Toxicol. 1990;44(2):224-229. doi:10.1007/BF01700140
19. Guo, Y. L. L., Yu, M. L., Hsu, C. C., & Rogan, W. J. (1999). Chloracne, goiter, arthritis, and anemia after polychlorinated biphenyl poisoning: 14-year follow-up of the Taiwan Yucheng cohort. Environmental Health Perspectives, 107(9), 715-719. doi:Doi 10.2307/3434656
20. Abella V, Santoro A, Scotece M, et al. Non-dioxin-like polychlorinated biphenyls (PCB 101, PCB 153 and PCB 180) induce chondrocyte cell death through multiple pathways. Toxicol Lett. 2015;234(1):13-19. doi:10.1016/j.toxlet.2015.02.001
21. Lee HG, Yang JH. PCB126 induces apoptosis of chondrocytes via ROS-dependent pathways. Osteoarthritis Cartilage. 2012;20(10):1179-1185. doi:10.1016/j.joca.2012.06.004
22. Kobayashi S, Okamoto H, Iwamoto T, et al. A role for the aryl hydrocarbon receptor and the dioxin TCDD in rheumatoid arthritis. Rheumatology (Oxford). 2008;47(9):1317-1322. doi:10.1093/rheumatology/ken259
23. Lee DH, Steffes M, Jacobs DR. Positive associations of serum concentration of polychlorinated biphenyls or organochlorine pesticides with self-reported arthritis, especially rheumatoid type, in women. Environ Health Perspect. 2007;115(6):883-888. doi:10.1289/ehp.9887
24. Turner W., DiPietro E., Lapeza C., Green V., Gill J., Patterson, D.G. , Jr. A fast universal automated cleanup system for the isotope-dilution highresolution mass spectrometric analysis of pcdds, pcdfs, coplanar pcbs, pcb congeners, and persistent pesticides from the same serum sample. Organohalogen compounds 31: 26-31 (1997).
25. Patterson DG Jr, Wong LY, Turner WE, et al. Levels in the U.S. population of those persistent organic pollutants (2003-2004) included in the Stockholm Convention or in other long range transboundary air pollution agreements. Environ Sci Technol. 2009;43(4):1211-1218. doi:10.1021/es801966w
26. Carpenter DO. Exposure to and health effects of volatile PCBs. Rev Environ Health. 2015;30(2):81-92. doi:10.1515/reveh-2014-0074
27. ATSDR, Thallium. "ATSDR (Agency for toxic substances and disease registry)." Prepared by clement international corp., under contract 205 (2000): 88-0608.
28. Kanagawa Y, Matsumoto S, Koike S, et al. Association of clinical findings in Yusho patients with serum concentrations of polychlorinated biphenyls, polychlorinated quarterphenyls and 2,3,4,7,8-pentachlorodibenzofuran more than 30 years after the poisoning event. Environ Health. 2008;7:47. Published 2008 Oct 2. doi:10.1186/1476-069X-7-47
29. Guo YL, Yu ML, Hsu CC, Rogan WJ. Chloracne, goiter, arthritis, and anemia after polychlorinated biphenyl poisoning: 14-year follow-Up of the Taiwan Yucheng cohort. Environ Health Perspect. 1999;107(9):715-719. doi:10.1289/ehp.99107715
30. Li MC, Tsai PC, Chen PC, Hsieh CJ, Leon Guo YL, Rogan WJ. Mortality after exposure to polychlorinated biphenyls and dibenzofurans: 30 years after the "Yucheng accident". Environ Res. 2013;120:71-75. doi:10.1016/j.envres.2012.09.003
31. Azamar-Llamas D, Hernández-Molina G, Ramos-Ávalos B, Furuzawa-Carballeda J. Adipokine contribution to the pathogenesis of osteoarthritis. Mediators Inflamm. 2017;2017:5468023. doi:10.1155/2017/5468023
32. Valentine, R. J., Vieira, V. J., Woods, J. A., & Evans, E. M. (2009). Stronger relationship between central adiposity and C-reactive protein in older women than men. Menopause, 16(1), 84-89
33. Khera A, McGuire DK, Murphy SA, et al. Race and gender differences in C-reactive protein levels. J Am Coll Cardiol. 2005;46(3):464-469. doi:10.1016/j.jacc.2005.04.051
34. Giles JT, Bartlett SJ, Andersen R, Thompson R, Fontaine KR, Bathon JM. Association of body fat with C-reactive protein in rheumatoid arthritis. Arthritis Rheum. 2008;58(9):2632-2641. doi:10.1002/art.23766.
35. Tabb MM, Kholodovych V, Grün F, Zhou C, Welsh WJ, Blumberg B. Highly chlorinated PCBs inhibit the human xenobiotic response mediated by the steroid and xenobiotic receptor (SXR). Environ Health Perspect. 2004;112(2):163-169. doi:10.1289/ehp.6560
36. Al-Salman F, Plant N. Non-coplanar polychlorinated biphenyls (PCBs) are direct agonists for the human pregnane-X receptor and constitutive androstane receptor, and activate target gene expression in a tissue-specific manner. Toxicol Appl Pharmacol. 2012;263(1):7-13. doi:10.1016/j.taap.2012.05.016
37. Kamata R, Shiraishi F, Kageyama S, Nakajima D. Detection and measurement of the agonistic activities of PCBs and mono-hydroxylated PCBs to the constitutive androstane receptor using a recombinant yeast assay. Toxicol In Vitro. 2015;29(7):1859-1867. doi:10.1016/j.tiv.2015.07.021
38. Kamata R, Nakajima D, Shiraishi F. Measurement of the agonistic activities of monohydroxylated polychlorinated biphenyls at the retinoid X and retinoic acid receptors using recombinant yeast cells. Toxicol In Vitro. 2019;57:9-17. doi:10.1016/j.tiv.2019.01.022
39. Johnson CD, Balagurunathan Y, Tadesse MG, et al. Unraveling gene-gene interactions regulated by ligands of the aryl hydrocarbon receptor. Environ Health Perspect. 2004;112(4):403-412. doi:10.1289/ehp.6758
40. Maier MS, Legare ME, Hanneman WH. The aryl hydrocarbon receptor agonist 3,3',4,4',5-pentachlorobiphenyl induces distinct patterns of gene expression between hepatoma and glioma cells: chromatin remodeling as a mechanism for selective effects. Neurotoxicology. 2007;28(3):594-612.