Skip to main content
SpringerLink
Log in

Relationship Between Markers of Chronic Inflammation and Copper Nutritional Status in Obese Women

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Adipose tissue dysfunction causes the development of metabolic complications, such as low-grade chronic inflammation, which may to alter copper homeostasis in obese individuals. Thus, the objective of this study is to analyze the relationship between markers of chronic inflammation and copper nutritional status in obese women. Cross-sectional study involved women aged 20–50 years, divided into two groups: case (BMI > 35 kg/m2) and control (18.5 > BMI > 24.9 kg/m2). Plasma and erythrocyte copper concentrations were determined by inductively coupled plasma optical emission spectrometry (ICP-OES) method. Activity of superoxide dismutase (SOD) enzyme in the erythrocytes was determined with an automatic biochemical analyzer. Serum concentrations of interleukin (IL)-6, IL-8, IL-12, IL-10, and IL-1β and tumor necrosis factor-alpha (TNF-α) were determined by using flow cytometer. Serum IL-6 concentrations were 105% higher in the case group compared to eutrophic women. Plasma copper concentrations were 20.5% higher, and erythrocyte copper concentrations were 23.5% lower in patients with obesity. In addition, erythrocyte SOD activity was 20% lower in obese participants when compared to eutrophic women. Our study identified significant negative correlation between the cytokines TNF-α and IL-10 and the SOD activity in the case group, suggesting a possible influence of chronic inflammation on copper distribution in obese individuals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. World Health Organization. Fact sheet on obesity and overweight [Internet]. 2021 [access in 2021 Sep 11]. Available in: http://www.who.int/mediacentre/factsheets/fs311/en/.

  2. Ramos-Lopez O, Milagro FI, Allayee H, Chmurzynska A, Choi MS, Curi R et al (2017) Guide for current nutrigenetic, nutrigenomic, and nutriepigenetic approaches for precision nutrition involving the prevention and management of chronic diseases associated with obesity. J Nutrigenet Nutrigenomics 10:43–62. https://doi.org/10.1159/000477729

    Article  CAS  PubMed  Google Scholar 

  3. Warolin J, Coenen KR, Kantor JL, Whitaker LE, Wang L, Acra SA, Roberts LJ 2nd, Buchowski MS (2014) The relationship of oxidative stress, adiposity and metabolic risk factors in healthy Black and White American youth. Pediatr Obes 9:43–52. https://doi.org/10.1111/j.2047-6310.2012.00135.x

    Article  CAS  PubMed  Google Scholar 

  4. Karczewski J, Śledzińska E, Baturo A, Jończyk I, Maleszko A, Samborski P, Begier-Krasińska B, Dobrowolska A (2018) Obesity and inflammation. Eur Cytokine Netw 29:83–94. https://doi.org/10.1684/ecn.2018.0415

    Article  CAS  PubMed  Google Scholar 

  5. Pereira TC, Campos MM, Bogo MR (2016) Copper toxicology, oxidative stress and inflammation using zebrafish as experimental model. J Appl Toxicol 36:876–885

    Article  CAS  PubMed  Google Scholar 

  6. Yang H, Liu CN, Wolf RM, Ralle M, Dev S, Pierson H, Askin F, Steele KE, Magnuson TH, Schweitzer MA, Wong GW, Lutsenko S (2019) Obesity is associated with copper elevation in serum and tissues. Metallomics 11:1363–1371. https://doi.org/10.1039/c9mt00148d

    Article  CAS  PubMed  Google Scholar 

  7. Fan Y, Zhang C, Bu J (2017) Relationship between selected serum metallic elements and obesity in children and adolescent in the U.S. Nutrients 9:104. https://doi.org/10.3390/nu9020104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Tinkov AA, Bogdański P, Skrypnik D, Skrypnik K, Skalny AV, Aaseth J, Skalnaya MG, Suliburska J (2021) Trace element and mineral levels in serum, hair, and urine of obese women in relation to body composition, blood pressure, lipid profile, and insulin resistance. Biomolecules 11:689. https://doi.org/10.3390/biom11050689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lima SC, Arrais RF, Sales CH, Almeida MG, de Sena KC, Oliveira VT, de Andrade AS, Pedrosa LF (2006) Assessment of copper and lipid profile in obese children and adolescents. Biol Trace Elem Res 114:19–29. https://doi.org/10.1385/BTER:114:1:19

    Article  CAS  PubMed  Google Scholar 

  10. Habib SA, Saad EA, Elsharkawy AA, Attia ZR (2015) Pro-inflammatory adipocytokines, oxidative stress, insulin, Zn and Cu: interrelations with obesity in Egyptian non-diabetic obese children and adolescents. Adv Med Sci 60:179–185. https://doi.org/10.1016/j.advms.2015.02.002

    Article  PubMed  Google Scholar 

  11. Gu K, Li X, Xiang W, Jiang X (2020) The relationship between serum copper and overweight/obesity: a meta-analysis. Biol Trace Elem Res 194:336–347. https://doi.org/10.1007/s12011-019-01803-6

    Article  CAS  PubMed  Google Scholar 

  12. Song X, Wang W, Li Z, Zhang D (2018) Association between serum copper and serum lipids in adults. Ann Nutr Metab 73:282–289. https://doi.org/10.1159/000494032

    Article  CAS  PubMed  Google Scholar 

  13. Brazil. Ministry of Health. Resolution Nº. 466/12. 2012. Approves guidelines and regulatory norms for research involving human beings. Official Diary of the Union. Brasilia

  14. Brazil. Ministry of Health. Health Care Department. Department of Primary Care. 2011 Guidelines for the collection and analysis of anthropometric data in health services: Technical Standard of the Food and Nutrition Surveillance System - SISVAN / Ministry of Health, Department of Health Care, Department of Primary Care. – Brasília: Ministry of Health

  15. World Health Organization (2000) Obesity: preventing and managing the global epidemic. Technical report series, Geneva 894:9

    Google Scholar 

  16. World Health Organization. 2011 Waist circumference and waist–hip ratio: report of a WHO Expert Consultation. Geneva

  17. Anção MS, Cuppari L, Draine AS, Singulem D. 2002 Nutwin Nutrition Support Program: version 1.5. São Paulo: Department of Health Informatics, SPDM, Unifesp/EPM. 1 CDROM.

  18. Nucleus of studies and research in food – NEPA. 2011 Brazilian Food Composition Table - TACO. 4. ed. Campinas: NEPA. 164 p.

  19. Brazil. Brazilian Institute of Geography and Statistics – IBGE. 2011. Household budget survey 2008–2009: analysis of personal food consumption in Brazil. Rio de Janeiro: IBGE, Coordination of Work and Income

  20. Fisberg RM, Marchioni DML, Slater B, Martini LA. 2005. Food surveys: methods and scientific basis. São Paulo: Manole

  21. Jaime PC, Latorre MRDO, Fornés NS, Zerbini CAF (2003) Comparative study among two methods for energy adjustment for nutrient intake. Nutrire 26:11–18

    Google Scholar 

  22. Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:17–27. https://doi.org/10.1093/oxfordjournals.aje.a114366

    Article  CAS  PubMed  Google Scholar 

  23. Whitehouse RC, Prasad AS, Rabbani PI, Cossack ZT (1982) Zinc in plasma, neutrophils, lymphocytes, and erythrocytes as determined by flameless atomic absorption spectrophotometry. Clin Chem 28:475–480

    Article  CAS  PubMed  Google Scholar 

  24. Błażewicz A, Klatka M, Astel A, Partyka M, Kocjan R (2013) Differences in trace metal concentrations (Co, Cu, Fe, Mn, Zn, Cd, And Ni) in whole blood, plasma, and urine of obese and nonobese children. Biol Trace Elem Res 155:190–200. https://doi.org/10.1007/s12011-013-9783-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Harrington JM, Young DJ, Essader AS, Sumner SJ, Levine KE (2014) Analysis of human serum and whole blood for mineral content by ICP-MS and ICP-OES: development of a mineralomics method. Biol Trace Elem Res 160:132–142. https://doi.org/10.1007/s12011-014-0033-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Niedzielski P, Siepak M (2003) Analytical methods for determining arsenic, antimony and selenium in environmental samples. Pol J Environ Stud 12:653–667

    CAS  Google Scholar 

  27. Burtis CA, Ashwood ER (1998) Fundamentals of clinical chemistry. Guanabara Koogan, Rio de Janeiro

    Google Scholar 

  28. Vitoux D, Arnaud J, Chappuis P (1999) Are copper, zinc and selenium in erythrocytes valuable biological indexes of nutrition and pathology? J Trace Elem Med Biol 13:113–128. https://doi.org/10.1016/S0946-672X(99)80001-7

    Article  CAS  PubMed  Google Scholar 

  29. Todendi PF, Possuelo LG, Klinger EI, Reuter CP, Burgos MS, Moura DJ, Fiegenbaum M, Valim AR (2016) Low-grade inflammation markers in children and adolescents: influence of anthropometric characteristics and CRP and IL6 polymorphisms. Cytokine 88:177–183. https://doi.org/10.1016/j.cyto.2016.09.007

    Article  CAS  PubMed  Google Scholar 

  30. Nikseresht M (2018) Comparison of serum cytokine levels in men who are obese or men who are lean: effects of nonlinear periodized resistance training and obesity. J Strength Cond Res 32:1787–1795. https://doi.org/10.1519/JSC.0000000000002039

    Article  PubMed  Google Scholar 

  31. Lasselin J, Magne E, Beau C, Ledaguenel P, Dexpert S, Aubert A, Layé S, Capuron L (2014) Adipose inflammation in obesity: relationship with circulating levels of inflammatory markers and association with surgery-induced weight loss. J Clin Endocrinol Metab 99:53–61. https://doi.org/10.1210/jc.2013-2673

    Article  Google Scholar 

  32. Li F, Li Y, Duan Y, Hu CA, Tang Y, Yin Y (2017) Myokines and adipokines: iInvolvement in the crosstalk between skeletal muscle and adipose tissue. Cytokine Growth Factor Rev 33:73–82. https://doi.org/10.1016/j.cytogfr.2016.10.003

    Article  CAS  PubMed  Google Scholar 

  33. Dorneles GP, Haddad DO, Fagundes VO, Vargas BK, Kloecker A, Romão PR, Peres A (2016) High intensity interval exercise decreases IL-8 and enhances the immunomodulatory cytokine interleukin-10 in lean and overweight-obese individuals. Cytokine 77:1–9. https://doi.org/10.1016/j.cyto.2015.10.003

    Article  CAS  PubMed  Google Scholar 

  34. Straczkowski M, Dzienis-Straczkowska S, Stêpieñ A, Kowalska I, Szelachowska M, Kinalska I (2002) Plasma interleukin-8 concentrations are increased in obese subjects and related to fat mass and tumor necrosis factor-alpha system. J Clin Endocrinol Metab 87:4602–4606. https://doi.org/10.1210/jc.2002-020135

    Article  CAS  PubMed  Google Scholar 

  35. Kim CS, Park HS, Kawada T, Kim JH, Lim D, Hubbard NE, Kwon BS, Erickson KL, Yu R (2006) Circulating levels of MCP-1 and IL-8 are elevated in human obese subjects and associated with obesity-related parameters. Int J Obes (Lond) 30:1347–1355. https://doi.org/10.1038/sj.ijo.0803259

    Article  CAS  PubMed  Google Scholar 

  36. Di Toro A, Marotta A, Todisco N, Ponticiello E, Collini R, Di Lascio R, Perrone L (1997) Unchanged iron and copper and increased zinc in the blood of obese children after two hypocaloric diets. Biol Trace Elem Res 57:97–104. https://doi.org/10.1007/BF02778192

    Article  PubMed  Google Scholar 

  37. Phelan S, Abrams B, Wing RR (2019) Prenatal intervention with partial meal replacement improves micronutrient intake of pregnant women with obesity. Nutrients 11:1071. https://doi.org/10.3390/nu11051071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Bo S, Durazzo M, Gambino R, Berutti C, Milanesio N, Caropreso A, Gentile L, Cassader M, Cavallo-Perin P, Pagano G (2008) Associations of dietary and serum copper with inflammation, oxidative stress, and metabolic variables in adults. J Nutr 138:305–310. https://doi.org/10.1093/jn/138.2.305

    Article  CAS  PubMed  Google Scholar 

  39. Bénetier C, Bertin M, Calamassi-Tran G, Dubuisson C, Dufour A, Gauchard F, et al (2009). Etude Individuelle Nationale des Consommations Alimentaires 2 (INCA 2) (2006–2007). [Google Scholar]

  40. Oestreicher P, Cousins RJ (1985) Copper and zinc absorption in the rat: mechanism of mutual antagonism. J Nutr 115:159–166. https://doi.org/10.1093/jn/115.2.159

    Article  CAS  PubMed  Google Scholar 

  41. Feitosa MCP, Lima VBD, Neto JMM, Marreiro DD (2013) Plasma concentration of IL-6 and TNF-alpha and its relationship with zincemia in obese women. Rev Assoc Med Bras 59:429–434. https://doi.org/10.1016/j.ramb.2013.03.003

    Article  PubMed  Google Scholar 

  42. Pannecoeck R, Serruys D, Benmeridja L, Delanghe JR, van Geel N, Speeckaert R, Speeckaert MM (2015) Vascular adhesion protein-1: role in human pathology and application as a biomarker. Crit Rev Clin Lab Sci 52:284–300. https://doi.org/10.3109/10408363.2015.1050714

    Article  CAS  PubMed  Google Scholar 

  43. Hordyjewska A, Popiołek Ł, Kocot J (2014) The many “faces” of copper in medicine and treatment. Biometals 27:611–621. https://doi.org/10.1007/s10534-014-9736-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Connaughton RM, McMorrow AM, McGillicuddy FC, Lithander FE, Roche HM (2016) Impact of anti-inflammatory nutrients on obesity-associated metabolic-inflammation from childhood through to adulthood. Proc Nutr Soc 75:115–124. https://doi.org/10.1017/S0029665116000070

    Article  PubMed  Google Scholar 

  45. Engström G, Stavenow L, Hedblad B, Lind P, Eriksson KF, Janzon L, Lindgärde F (2003) Inflammation-sensitive plasma proteins, diabetes, and mortality and incidence of myocardial infarction and stroke: a population-based study. Diabetes 52:442–447. https://doi.org/10.2337/diabetes.52.2.442

    Article  PubMed  Google Scholar 

  46. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87

    Article  CAS  PubMed  Google Scholar 

  47. Burkitt MJ, Milne L, Raafat A (2001) A simple, highly sensitive and improved method for the measurement of bleomycin-detectable iron: the ‘catalytic iron index’and its value in the assessment of iron status in haemochromatosis. Clin Sci 100:239–247

    Article  CAS  Google Scholar 

  48. Jaksic M, Martinovic M, Gligorovic-Barhanovic N, Vujacic A, Djurovic D, Nedovic-Vukovic M (2019) Association between inflammation, oxidative stress, vitamin D, copper and zinc with pre-obesity and obesity in school children from the city of Podgorica, Montenegro. J Pediatr Endocrinol Metab 32:951–957. https://doi.org/10.1515/jpem-2019-0086

    Article  CAS  PubMed  Google Scholar 

  49. Brito GHR., Tajra VEF, Rocha dos Santos L, Melo SRDS, Morais JBS, Soares Severo, J, Batista Beserra J (2018). Copper concentrations in obese women and their relationship with a marker of lipid peroxidation. Nutr. clín. diet. Hosp: 134–139.

  50. Jardim-Botelho A, Queiroz Gurgel R, Simeone Henriques G, Dos Santos CB, Afonso Jordão A, Nascimento Faro F, Silveira Souto FM, Rodrigues Santos AP, Eduardo Cuevas L (2016) Micronutrient deficiencies in normal and overweight infants in a low socio-economic population in north-east Brazil. Paediatr Int Child Health 36:198–202. https://doi.org/10.1179/2046905515Y.0000000035

    Article  PubMed  Google Scholar 

  51. Amirkhizi F, Siassi F, Djalali M, Shahraki SH (2014) Impaired enzymatic antioxidant defense in erythrocytes of women with general and abdominal obesity. Obes Res Clin Pract 8:26–34. https://doi.org/10.1016/j.orcp.2012.07.004

    Article  Google Scholar 

  52. Ozata M, Mergen M, Oktenli C, Aydin A, Sanisoglu SY, Bolu E, Yilmaz MI, Sayal A, Isimer A, Ozdemir IC (2002) Increased oxidative stress and hypozincemia in male obesity. Clin Biochem 35:627–631. https://doi.org/10.1016/s0009-9120(02)00363-6

    Article  CAS  PubMed  Google Scholar 

  53. Olusi S (2002) Obesity is an independent risk factor for plasma lipid peroxidation and depletion of erythrocyte cytoprotectic enzymes in humans. Int J Obes Relat Metab Disord 26:1159–1166

    Article  CAS  PubMed  Google Scholar 

  54. Chen SJ, Yen CH, Huang YC, Lee BJ, Hsia S, Lin PT (2012) Relationships between inflammation, adiponectin, and oxidative stress in metabolic syndrome. PLoS ONE 7:e45693. https://doi.org/10.1371/journal.pone.0045693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Aguiar SS, Sousa CV, Deus LA, Rosa TS, Sales MM, Neves RVP, Barbosa LP, Santos PA, Campbell CS, Simões HG (2020) Oxidative stress, inflammatory cytokines and body composition of master athletes: the interplay. Exp Gerontol 130:110806. https://doi.org/10.1016/j.exger.2019.110806

    Article  CAS  PubMed  Google Scholar 

  56. de Waal MR, Abrams J, Bennett B, Figdor CG, de Vries JE (1991) Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 174:1209–1220. https://doi.org/10.1084/jem.174.5.1209

    Article  Google Scholar 

  57. Romieu I, Dossus L, Barquera S, Blottière HM, Franks PW, Gunter M et al (2017) Energy balance and obesity: what are the main drivers? Cancer Causes Control 28:247–258. https://doi.org/10.1007/s10552-017-0869-z

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was funded by the National Coordination of Higher Education Personnel Training Programs (CAPES – Brazil) (Finance Code 001).

Author information

Authors and Affiliations

  1. Department of Nutrition, Federal University of Piauí, Teresina, Piauí, Brazil

    Mickael de Paiva Sousa, Larissa Cristina Fontenelle, Thayanne Gabryelle Visgueira de Sousa, Loanne Rocha dos Santos, Kyria Jayanne Clímaco Cruz, Tamires da Cunha Soares & Dilina do Nascimento Marreiro

  2. Department of Pharmacy, Federal University of Piauí, Teresina, Piauí, Brazil

    Débora Cavalcante Braz

  3. Department of Biochemistry and Pharmacology, Federal University of Piauí, Teresina, Piauí, Brazil

    João Marcelo de Castro e Sousa

  4. Department of Nutrition, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil

    Gilberto Simeone Henriques

  5. Leishmaniasis Research Laboratory, Federal University of Piauí, Teresina, Piauí, Brazil

    Vladimir Costa Silva & Carlos Henrique Nery Costa

Authors
  1. Mickael de Paiva Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Larissa Cristina Fontenelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thayanne Gabryelle Visgueira de Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Loanne Rocha dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kyria Jayanne Clímaco Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tamires da Cunha Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Débora Cavalcante Braz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. João Marcelo de Castro e Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gilberto Simeone Henriques
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Vladimir Costa Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Carlos Henrique Nery Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Dilina do Nascimento Marreiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: MPS and DNM; methodology: MPS, LCF, KJCC, TGVS and DNM; resources: DNM, GSH, DCB and JMCS; investigation: MPS, LCF, LRS, TGVS and TCS; formal analysis: MPS, DCB, and GSH; Visualization and writing — original draft: MPS; writing — review and editing: MPS and DNM; project administration and supervision: DNM.

Corresponding author

Correspondence to Mickael de Paiva Sousa.

Ethics declarations

Ethics Approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Federal University of Piauí (Date: 12 April 2017/No 2.014.100). Informed consent was obtained from all individual participants included in the study.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Paiva Sousa, M., Fontenelle, L.C., de Sousa, T.G.V. et al. Relationship Between Markers of Chronic Inflammation and Copper Nutritional Status in Obese Women. Biol Trace Elem Res 201, 3133–3143 (2023). https://doi.org/10.1007/s12011-022-03407-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-022-03407-z

Keywords

Search

Navigation