Upregulation of CCL7, CCL20, CXCL2, IL-1β, IL-6 and MMP-9 in Skin Samples of PCB Exposed Individuals—A Preliminary Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Group
2.2. Determination of PCB
2.3. RNA Isolation and qRT-PCR
2.4. Statistical Analysis
3. Results
3.1. Discriptive Statistics of the Cohort
3.2. Confounding Factors
3.3. Regulation of Cutaneous Genes
3.4. Regulation of Cutaneous Genes Correlated with Oxidative Stress and the Epidermal Growth Factor (Nrf2 and EPGN)
4. Discussion
4.1. Regulation of CCL7, CCL20, CXCL2, IL-1β, MMP-9 and IL-6
4.2. Nrf2 and Epigen
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Van den Berg, M.; Denison, M.S.; Birnbaum, L.S.; Devito, M.J.; Fiedler, H.; Falandysz, J.; Rose, M.; Schrenk, D.; Safe, S.; Tohyama, C.; et al. Polybrominated dibenzo-p-dioxins, dibenzofurans, and biphenyls: Inclusion in the toxicity equivalency factor concept for dioxin-like compounds. Toxicol. Sci. Off. J. Soc. Toxicol. 2013, 133, 197–208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leijs, M.M.; Koppe, J.G.; Olie, K.; Van Aalderen, W.M.; De Voogt, P.; Tusscher, G.W.T. Effects of Dioxins, PCBs, and PBDEs on Immunology and Hematology in Adolescents. Environ. Sci. Technol. 2009, 43, 7946–7951. [Google Scholar] [CrossRef] [PubMed]
- Leijs, M.M.; ten Tusscher, G.W.; Olie, K.; van Teunenbroek, T.; van Aalderen, W.M.; de Voogt, P.; Vulsma, T.; Bartonova, A.; von Krauss, M.K.; Mosoiu, C.; et al. Thyroid hormone metabolism and environmental chemical exposure. Environ Health 2012, 11 (Suppl. 1), S10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brinkman, U.A.T.; De Kok, A. Halogenated Biphenyls, Terphenyls, Naphtalenes, Dibenzodioxins and Related Products; Kimbrough, R.D., Jensen, A.A., Eds.; Elsevier Science Publisher: New York, NY, USA, 1989; pp. 3–45. [Google Scholar]
- Lauby-Secretan, B.; Loomis, D.; Grosse, Y.; El Ghissassi, F.; Bouvard, V.; Benbrahim-Tallaa, L.; Guha, N.; Baan, R.; Mattock, H.; Straif, K. Carcinogenicity of polychlorinated biphenyls and polybrominated biphenyls. Lancet Oncol. 2013, 14, 287–288. [Google Scholar] [CrossRef] [Green Version]
- Rogan, W.; Gladen, B.; Hung, K.; Koong, S.; Shih, L.; Taylor, J.; Wu, Y.; Yang, D.; Ragan, N.; Hsu, C. Congenital poisoning by polychlorinated biphenyls and their contaminants in Taiwan. Science 1988, 241, 334–336. [Google Scholar] [CrossRef] [Green Version]
- Ritter, R.; Scheringer, M.; MacLeod, M.; Moeckel, C.; Jones, K.C.; Hungerbühler, K. Intrinsic Human Elimination Half-Lives of Polychlorinated Biphenyls Derived from the Temporal Evolution of Cross-Sectional Biomonitoring Data from the United Kingdom. Environ. Health Perspect. 2011, 119, 225–231. [Google Scholar] [CrossRef]
- Leijs, M.; Van Teunenbroek, T.; Olie, K.; Koppe, J.; Tusscher, G.T.; Van Aalderen, W.; De Voogt, P. Assessment of current serum levels of PCDD/Fs, dl-PCBs and PBDEs in a Dutch cohort with known perinatal PCDD/F exposure. Chemosphere 2008, 73, 176–181. [Google Scholar] [CrossRef]
- Wong, T.W.; Wong, A.H.; Nelson, E.A.S.; Qiu, H.; Ku, S.Y. Levels of PCDDs, PCDFs, and dioxin-like PCBs in human milk among Hong Kong mothers. Sci. Total. Environ. 2013, 463–464, 1230–1238. [Google Scholar] [CrossRef]
- Pang, S.; Cao, J.Q.; Katz, B.H.; Hayes, C.L.; Sutter, T.R.; Spink, D.C. Inductive and inhibitory effects of non-ortho-substituted polychlorinated biphenyls on estrogen metabolism and human cytochromes P450 1A1 and 1B1. Biochem. Pharmacol. 1999, 58, 29–38. [Google Scholar] [CrossRef]
- Leijs, M.K.; Koppe, J.G.; Kraus, T.; Baron, J.M.; Merk, H.F. Pops and Skin; Krutmann, J., Merk, H.F., Eds.; Springer: Berlin/Heidelberg, Germany, 2018; 170 p. [Google Scholar]
- Yoshimura, T. Yusho in Japan. Ind Health. 2003, 41, 139–148. [Google Scholar] [PubMed] [Green Version]
- Furue, M.; Tsuji, G. Chloracne and Hyperpigmentation Caused by Exposure to Hazardous Aryl Hydrocarbon Receptor Ligands. Int. J. Environ. Res. Public Health 2019, 16, 4864. [Google Scholar] [CrossRef] [Green Version]
- Saurat, J.-H.; Kaya, G.; Saxer-Sekulic, N.; Pardo, B.; Becker, M.; Fontao, L.; Mottu, F.; Carraux, P.; Pham, X.-C.; Barde, C.; et al. The Cutaneous Lesions of Dioxin Exposure: Lessons from the Poisoning of Victor Yushchenko. Toxicol. Sci. 2011, 125, 310–317. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Zhang, C.-M.; Coenraads, P.-J.; Ji, Z.-Y.; Chen, X.; Dong, L.; Ma, X.-M.; Han, W.; Tang, N.-J. Abnormal expression of MAPK, EGFR, CK17 and TGk in the skin lesions of chloracne patients exposed to dioxins. Toxicol. Lett. 2011, 201, 230–234. [Google Scholar] [CrossRef] [Green Version]
- Schafer, M.; Willrodt, A.H.; Kurinna, S.; Link, A.S.; Farwanah, H.; Geusau, A.; Gruber, F.; Sorg, O.; Huebner, A.J.; Roop, D.R.; et al. Activation of Nrf2 in keratinocytes causes chloracne (MADISH)-like skin disease in mice. EMBO Mol. Med. 2014, 6, 442–457. [Google Scholar] [CrossRef] [PubMed]
- Schettgen, T.; Gube, M.; Esser, A.; Alt, A.; Kraus, T. Plasma Polychlorinated Biphenyls (PCB) Levels of Workers in a Transformer Recycling Company, their Family Members, and Employees of Surrounding Companies. J. Toxicol. Environ. Health Part A 2012, 75, 414–422. [Google Scholar] [CrossRef]
- Kraus, T.; Gube, M.; Lang, J.; Esser, A.; Sturm, W.; Fimm, B.; Willmes, K.; Neulen, J.; Baron, J.; Merk, H.; et al. Surveillance Program for Former PCB-Exposed Workers of a Transformer and Capacitor Recycling Company, Family Members, Employees of Surrounding Companies, and Area Residents—Executive Summary. J. Toxicol. Environ. Health Part A 2012, 75, 1241–1247. [Google Scholar] [CrossRef]
- Haase, H.; Fahlenkamp, A.; Schettgen, T.; Esser, A.; Gube, M.; Ziegler, P.; Kraus, T.; Rink, L. Immunotoxicity Monitoring in a Population Exposed to Polychlorinated Biphenyls. Int. J. Environ. Res. Public Health 2016, 13, 295. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leijs, M.M.; Esser, A.; Amann, P.M.; Schettgen, T.; Gube, M.; Merk, H.F.; Kraus, T.; Baron, J.M. Hyperpigmentation and higher incidence of cutaneous malignancies in moderate-high PCB- and dioxin exposed individuals. Environ. Res. 2018, 164, 221–228. [Google Scholar] [CrossRef] [PubMed]
- Leijs, M.M.; Gan, L.; De Boever, P.; Esser, A.; Amann, P.M.; Ziegler, P.; Fietkau, K.; Schettgen, T.; Kraus, T.; Merk, H.F.; et al. Altered Gene Expression in Dioxin-Like and Non-Dioxin-Like PCB Exposed Peripheral Blood Mononuclear Cells. Int. J. Environ. Res. Public Health 2019, 16, 2090. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schettgen, T.; Gube, M.; Alt, A.; Fromme, H.; Kraus, T. Pilot study on the exposure of the German general population to non-dioxin-like and dioxin-like PCBs. Int. J. Hyg. Environ. Health 2011, 214, 319–325. [Google Scholar] [CrossRef] [PubMed]
- Wittsiepe, J.; Wilhelm, M.; Kraus, T. Levels of Polychlorinated Dibenzo-p-Dioxins and Dibenzofurans (PCDD/F) in Blood Samples of Occupationally Exposed Workers from a Transformer Recycling Plant in Dortmund, Germany—Initial Findings. J. Toxicol. Environ. Health Part A 2012, 75, 423–428. [Google Scholar] [CrossRef]
- Skazik, C.; Amann, P.M.; Heise, R.; Marquardt, Y.; Czaja, K.; Kim, A.; Rühl, R.; Kurschat, P.; Merk, H.F.; Bickers, D.R.; et al. Downregulation of STRA6 expression in epidermal keratinocytes leads to hyperproliferation-associated differentiation in both in vitro and in vivo skin models. J. Investig. Dermatology. 2014, 134, 1579–1588. [Google Scholar] [CrossRef] [Green Version]
- IBM-Corporation. IBM SPSS V23 Statistics for Windows, Version 23 ed.; IBM-Corporation: Armonk, NY, USA, 2015. [Google Scholar]
- Benjamini, Y.; Hochberg, Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc. Ser. B Statistical Methodol. 1995, 57, 289–300. [Google Scholar] [CrossRef]
- Leijs, M.M.; Esser, A.; Amann, P.M.; Schettgen, T.; Heise, R.; Fietkau, K.; Gube, M.; Merk, H.F.; Kraus, T.; Baron, J.M. Expression of CYP1A1, CYP1B1 and Il-1β in PBMCs and skin samples of PCB exposed individuals. Sci. Total Environ. 2018, 642, 1429–1438. [Google Scholar] [CrossRef]
- Zgheib, E.; Limonciel, A.; Jiang, X.; Wilmes, A.; Wink, S.; Van De Water, B.; Kopp-Schneider, A.; Bois, F.Y.; Jennings, P. Investigation of Nrf2, AhR and ATF4 Activation in Toxicogenomic Databases. Front. Genet. 2018, 9, 429. [Google Scholar] [CrossRef] [PubMed]
- Ishida, M.; Mikami, S.; Kikuchi, E.; Kosaka, T.; Miyajima, A.; Nakagawa, K.; Mukai, M.; Okada, Y.; Oya, M. Activation of the aryl hydrocarbon receptor pathway enhances cancer cell invasion by upregulating the MMP expression and is associated with poor prognosis in upper urinary tract urothelial cancer. Carcinogenesis 2009, 31, 287–295. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martinez, J.M.; Afshari, C.A.; Bushel, P.R.; Masuda, A.; Takahashi, T.; Walker, N.J. Differential toxicogenomic responses to 2,3,7,8-tetrachlorodibenzo-p-dioxin in malignant and nonmalignant human airway epithelial cells. Toxicol Sci. 2002, 69, 409–423. [Google Scholar] [CrossRef] [PubMed]
- Hennig, B.; Meerarani, P.; Slim, R.; Toborek, M.; Daugherty, A.; Silverstone, A.E.; Robertson, L.W. Proinflammatory properties of coplanar PCBs: In vitro and in vivo evidence. Toxicol Appl Pharmacol. 2002, 181, 174–183. [Google Scholar] [CrossRef] [PubMed]
- Brouwer, A.; Longnecker, M.P.; Birnbaum, L.S.; Cogliano, J.; Kostyniak, P.; Moore, J. Characterization of potential endocrine-related health effects at low-dose levels of exposure to PCBs. Environ. Health Perspect. 1999, 107 (Suppl. 4), 639–649. [Google Scholar]
- Acharyya, S.; Oskarsson, T.; Vanharanta, S.; Malladi, S.; Kim, J.; Morris, P.G.; Manova-Todorova, K.; Leversha, M.; Hogg, N.; Seshan, V.E.; et al. A CXCL1 Paracrine Network Links Cancer Chemoresistance and Metastasis. Cell 2012, 150, 165–178. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arima, Y.; Harada, M.; Kamimura, D.; Park, J.-H.; Kawano, F.; Yull, F.E.; Kawamoto, T.; Iwakura, Y.; Betz, U.A.; Márquez, G.; et al. Regional Neural Activation Defines a Gateway for Autoreactive T Cells to Cross the Blood-Brain Barrier. Cell 2012, 148, 447–457. [Google Scholar] [CrossRef] [Green Version]
- Guo, Y.; Xu, F.; Lu, T.; Duan, Z.; Zhang, Z. Interleukin-6 signaling pathway in targeted therapy for cancer. Cancer Treat. Rev. 2012, 38, 904–910. [Google Scholar] [CrossRef]
- Xu, L.; Guo, X.; Li, N.; Pan, Q.; Ma, Y.Z. Effects of quercetin on Aroclor 1254-induced expression of CYP450 and cytokines in pregnant rats. J. Immunotoxicol. 2019, 16, 140–148. [Google Scholar] [CrossRef] [Green Version]
- Kumari, N.; Dwarakanath, B.S.; Das, A.; Bhatt, A.N. Role of interleukin-6 in cancer progression and therapeutic resistance. Tumor Biol. 2016, 37, 11553–11572. [Google Scholar] [CrossRef]
- Wu, C.-T.; Chen, M.-F.; Chen, W.-C.; Hsieh, C.-C. The role of IL-6 in the radiation response of prostate cancer. Radiat. Oncol. 2013, 8, 159. [Google Scholar] [CrossRef] [Green Version]
- Bastard, J.-P.; Jardel, C.; Delattre, J.; Hainque, B.; Bruckert, E.; Oberlin, F. Evidence for a Link Between Adipose Tissue Interleukin-6 Content and Serum C-Reactive Protein Concentrations in Obese Subjects. Circulation 1999, 99, 2221–2222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lou, J.; Wu, N.; Song, P.; Jin, L.; Gao, M.; Song, Y.; Tan, Y.; Liu, K. Chemokine (C-C motif) ligand 22 is down-regulated in a human B lymphoblastoid cell line by PCB153 and in residents from PCBs-contaminated areas. Mutat. Res. Toxicol. Environ. Mutagen. 2013, 752, 21–27. [Google Scholar] [CrossRef]
- Wunderlich, C.M.; Ackermann, P.J.; Ostermann, A.L.; Adams-Quack, P.; Vogt, M.C.; Tran, M.-L.; Nikolajev, A.; Waisman, A.; Garbers, C.; Theurich, S.; et al. Obesity exacerbates colitis-associated cancer via IL-6-regulated macrophage polarisation and CCL-20/CCR-6-mediated lymphocyte recruitment. Nat. Commun. 2018, 9, 1646. [Google Scholar] [CrossRef] [PubMed]
- Kuwatsuka, Y.; Shimizu, K.; Akiyama, Y.; Koike, Y.; Ogawa, F.; Furue, M. Yusho patients show increased serum IL-17, IL-23, IL-1beta, and TNFalpha levels more than 40 years after accidental polychlorinated biphenyl poisoning. J. Immunotoxicol. 2014, 11, 246–249. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsuji, G.; Takahara, M.; Uchi, H.; Takeuchi, S.; Mitoma, C.; Moroi, Y.; Furue, M. An environmental contaminant, benzo(a)pyrene, induces oxidative stress-mediated interleukin-8 production in human keratinocytes via the aryl hydrocarbon receptor signaling pathway. J. Dermatol. Sci. 2011, 62, 42–49. [Google Scholar] [CrossRef]
- Panteleyev, A.A.; Bickers, D.R. Dioxin-induced chloracne-reconstructing the cellular and molecular mechanisms of a classic environmental disease. Exp. Dermatol. 2006, 15, 705–730. [Google Scholar] [CrossRef] [PubMed]
- Imbeault, P.; Findlay, C.S.; Robidoux, M.A.; Haman, F.; Blais, J.M.; Tremblay, A.; Springthorpe, S.; Pal, S.; Seabert, T.; Krümmel, E.M.; et al. Dysregulation of cytokine response in Canadian First Nations communities: Is there an association with persistent organic pollutant levels? PLoS ONE 2012, 7, e39931. [Google Scholar]
- Huggett, J.F.; Dheda, K.; Bustin, S.; Zumla, P.S.A. Real-time RT-PCR normalisation; strategies and considerations. Genes Immun. 2005, 6, 279–284. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zimta, A.A.; Cenariu, D.; Irimie, A.; Magdo, L.; Nabavi, S.M.; Atanasov, A.G.; Berindan-Neagoe, I. The Role of Nrf2 Activity in Cancer Development and Progression. Cancers 2019, 11, 1755. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Descriptive | Age (n = 25) | BMI (n = 25) | Plasma ndl-PCB Levels (n = 25) μg/L | DL-PCB Levels (n = 25) µg/L | Dioxin Levels (n = 25) pg/g Fat |
---|---|---|---|---|---|
Mean (range) | 47.98 (29–87) | 28.8 (21.0–40.9) | 31.81 (2.15–178.4) | 6.12 (0.50–36.68) | 31.66 (5.55–109.66) |
Median | 48 | 28.3 | 16.99 | 2.75 | 23.83 |
Confounding Factors | MMP-9 | IL-1ß | CCL7 | CCL20 | CXCL2 | IL-6 | EPGN | NRF2 | |
---|---|---|---|---|---|---|---|---|---|
Age | ρ | −0.049 | 0.067 | 0.041 | 0.122 | −0.013 | −0.055 | −0.246 | −0.342 |
p-value | 0.815 | 0.749 | 0.846 | 0.562 | 0.950 | 0.795 | 0.310 | 0.152 | |
Smoking | ρ | −0.019 | −0.075 | 0.117 | −0.253 | 0.026 | −0.087 | 0.277 | 0.253 |
p-value | 0.929 | 0.720 | 0.578 | 0.223 | 0.900 | 0.680 | 0.250 | 0.297 | |
Serum lipids | ρ | 0.170 | −0.065 | 0.316 | −0.018 | 0.000 | −0.124 | −0.202 | 0.170 |
p-value | 0.417 | 0.756 | 0.124 | 0.930 | 1.000 | 0.614 | 0.408 | 0.417 | |
BMI | ρ | −0.042 | −0.218 | −0.049 | 0.038 | −0.177 | −0.101 | −0.099 | −0.061 |
p-value | 0.844 | 0.294 | 0.815 | 0.858 | 0.398 | 0.632 | 0.686 | 0.803 |
PCB | MMP-9 | IL-1ß | CCL7 | CCL20 | CXCL2 | IL-6 | EPGN | NRF2 | |
---|---|---|---|---|---|---|---|---|---|
PCB28 | ρ | 0.289 | 0.135 | 0.281 | 0.339 | 0.352 | 0.326 | 0.267 | −0.007 |
p-value | 0.278 | 0.594 | 0.278 | 0.278 | 0.278 | 0.278 | 0.358 | 0.977 | |
PCB 52 | ρ | 0.173 | 0.147 | 0.152 | 0.010 | 0.092 | 0.062 | 0.181 | −0.268 |
p-value | 0.774 | 0.774 | 0.774 | 0.961 | 0.879 | 0.879 | 0.774 | 0.774 | |
PCB101 | ρ | 0.103 | 0.109 | −0.011 | 0.130 | 0.139 | 0.246 | 0.227 | −0.310 |
p-value | 0.722 | 0.722 | 0.958 | 0.722 | 0.722 | 0.722 | 0.722 | 0.722 | |
PCB138 | ρ | 0.395 | 0.545 * | 0.265 | 0.354 | 0.428 | 0.327 | 0.210 | −0.102 |
p-value | 0.133 | 0.04 | 0.268 | 0.166 | 0.132 | 0.1776 | 0.445 | 0.679 | |
PCB153 | ρ | 0.392 | 0.560 * | 0.294 | 0.346 | 0.445 | 0.328 | 0.252 | −0.098 |
p-value | 0.139 | 0.032 | 0.205 | 0.176 | 0.104 | 0.176 | 0.341 | 0.689 | |
PCB180 | ρ | 0.375 | 0.537 * | 0.275 | 0.367 | 0.395 | 0.247 | 0.161 | −0.095 |
p-value | 0.142 | 0.048 | 0.293 | 0.142 | 0.142 | 0.312 | 0.582 | 0.700 | |
sum NDL-PCB | ρ | 0.439 | 0.587 * | 0.332 * | 0.438 | 0.494 * | 0.368 | 0.213 | −0.058 |
p-value | 0.056 | 0.016 | 0.014 | 0.056 | 0.048 | 0.114 | 0.435 | 0.814 | |
PCB105 | ρ | 0.358 | 0.321 | 0.314 | 0.295 | 0.452 | 0.505 | 0.254 | −0.032 |
p-value | 0.203 | 0.203 | 0.203 | 0.203 | 0.092 | 0.080 | 0.335 | 0.898 | |
PCB114 | ρ | 0.362 | 0.574 * | 0.261 | 0.430 | 0.455 | 0.376 | 0.097 | −0.163 |
p-value | 0.120 | 0.024 | 0.276 | 0.085 | 0.085 | 0.120 | 0.691 | 0.576 | |
PCB118 | ρ | 0.409 | 0.434 | 0.379 | 0.345 | 0.506 * | 0.502 * | 0.341 | −0.077 |
p-value | 0.084 | 0.080 | 0.099 | 0.121 | 0.044 | 0.044 | 0.175 | 0.753 | |
PCB156 | ρ | 0.332 * | 0.533 * | 0.226 | 0.354 | 0.355 | 0.234 | 0.125 | −0.171 |
p-value | 0.021 | 0.048 | 0.369 | 0.210 | 0.210 | 0.369 | 0.611 | 0.553 | |
PCB157 | ρ | 0.344 | 0.542 * | 0.247 | 0.398 | 0.404 | 0.279 | 0.069 | −0.111 |
p-value | 0.184 | 0.040 | 0.312 | 0.131 | 0.131 | 0.282 | 0.778 | 0.745 | |
PCB167 | ρ | 0.392 | 0.581 * | 0.264 | 0.413 | 0.418 | 0.314 | 0.107 | −0.118 |
p-value | 0.104 | 0.016 | 0.271 | 0.104 | 0.104 | 0.203 | 0.663 | 0.663 | |
PCB189 | ρ | 0.321 | 0.512 | 0.275 | 0.336 | 0.328 | 0.176 | 0.161 | −0.176 |
p-value | 0.234 | 0.072 | 0.293 | 0.234 | 0.234 | 0.510 | 0.510 | 0.510 | |
sum DL-PCBs (TEQ) | ρ | 0.506 * | 0.592 * | 0.418 | 0.407 | 0.564 * | 0.478 * | 0.274 | −0.054 |
p-value | 0.027 | 0.012 | 0.059 | 0.059 | 0.012 | 0.032 | 0.294 | 0.825 | |
sum PCBs (lipid adjusted) | ρ | 0.408 | 0.533 * | 0.325 | 0.348 | 0.516 * | 0.422 | 0.247 | −0.051 |
p-value | 0.086 | 0.032 | 0.149 | 0.141 | 0.032 | 0.086 | 0.351 | 0.836 | |
sum PCBs | ρ | 0.422 | 0.568 * | 0.32 | 0.407 | 0.488 | 0.381 | 0.199 | −0.091 |
p-value | 0.088 | 0.024 | 0.159 | 0.088 | 0.052 | 0.096 | 0.473 | 0.71 | |
WHO2005_ Teq_PCDD_F | ρ | 0.446 | 0.654 * | 0.475 | 0.639 * | 0.475 | 0.432 | 0.152 | 0.079 |
p-value | 0.144 | 0.040 | 0.144 | 0.040 | 0.144 | 0.1444 | 0.776 | 0.829 |
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Leijs, M.; Fietkau, K.; Merk, H.F.; Schettgen, T.; Kraus, T.; Esser, A. Upregulation of CCL7, CCL20, CXCL2, IL-1β, IL-6 and MMP-9 in Skin Samples of PCB Exposed Individuals—A Preliminary Study. Int. J. Environ. Res. Public Health 2021, 18, 9711. https://doi.org/10.3390/ijerph18189711
Leijs M, Fietkau K, Merk HF, Schettgen T, Kraus T, Esser A. Upregulation of CCL7, CCL20, CXCL2, IL-1β, IL-6 and MMP-9 in Skin Samples of PCB Exposed Individuals—A Preliminary Study. International Journal of Environmental Research and Public Health. 2021; 18(18):9711. https://doi.org/10.3390/ijerph18189711
Chicago/Turabian StyleLeijs, Marike, Katharina Fietkau, Hans F. Merk, Thomas Schettgen, Thomas Kraus, and André Esser. 2021. "Upregulation of CCL7, CCL20, CXCL2, IL-1β, IL-6 and MMP-9 in Skin Samples of PCB Exposed Individuals—A Preliminary Study" International Journal of Environmental Research and Public Health 18, no. 18: 9711. https://doi.org/10.3390/ijerph18189711