Dynamics of plasma micronutrient concentrations and their correlation with serum proteins and thyroid hormones in patients with paracoccidioidomycosis

English version

Autoři: Jeniffer Michelline de Oliveira Custódio ^aff001; Iasmim Mayumi Enokida ^aff002; Daniel Araujo Gonçalves ^aff003; Sandra Maria do Valle Leone de Oliveira ^aff004; James Venturini ^aff004; Lidia Raquel Carvalho ^aff005; Rinaldo Poncio Mendes ^aff006; Anamaria Mello Miranda Paniago ^aff004
Působiště autorů: Postgraduate Course in Health and Development of the Central West Region, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil ^aff001; Scientific initiation CNPq, Faculty of Medicine - FAMED, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brazil ^aff002; Department of Chemistry, Minas Gerais State University - UEMG, Ituiutaba, Minas Gerais, Brazil ^aff003; Faculty of Medicine- FAMED, Center for Biological and Health Sciences- CCBS, Federal University of Mato Grosso do Sul, Mato Grosso do Sul, Campo Grande, Brazil ^aff004; Department of Biostatistics, Institute of Biosciences, State University Paulista "Júlio de Mesquita Filho" -UNESP, Botucatu, São Paulo Brazil ^aff005; Department of Tropical Diseases, Botucatu Medical School, Universidade Estadual Paulista (UNESP), Botucatu, São Paulo, Brazil ^aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226609

Souhrn

Minerals, such as zinc, copper, and iron are reported to play roles in chronic infectious diseases; however, their role in paracoccidioidomycosis (PCM) remains unknown. This study aimed to examine the micronutrient dynamics and their correlation with serum proteins and thyroid hormones in patients with PCM. In 14 patients with PCM and 10 healthy subjects, we evaluated the body mass index (BMI) along with serum levels of hemoglobin, iron, ferritin, zinc, copper, magnesium, albumin, globulin, thyroid stimulating hormone (TSH), thyroxine (free T4), and triiodothyronine (T3). Evaluations were conducted at the first appointment, before treatment, and at the end of the first, second, fourth, and sixth month of PCM treatment. The control group was only evaluated once. We observed that before treatment, patients with PCM, had higher levels of copper and lower level of iron than those of the control group. After one month of treatment, the iron levels increased, whereas the levels of copper after six months of treatment. Reduction in inflammatory activity, indicated by the normalization of C-reactive protein, ferritin, albumin, and globulin levels, was observed during treatment. However, no correlation was observed between the serum levels of minerals and inflammatory activity or thyroid function in this study. In conclusion, our results showed higher serum copper levels in control group compared to those in pretreatment patients; the clinical importance of this observation should be investigated in further studies. After treatment, serum copper levels showed a tendency to decrease. In addition, serum iron levels were decreased at the stage of active disease, and were increased after treatment. Thus, serum iron levels can be used as a better biomarker for treatment control.

Klíčová slova:

Thyroid-stimulating hormone – Zinc – Albumins – Thyroid – Magnesium – Globulins – Iron – Paracoccidioidomycosis

Zdroje

1. Weiss G, Carver PL. Role of divalent metals in infectious disease susceptibility and outcome. Clin Microbiol Infect. 2018;24(1):16–23. doi: 10.1016/j.cmi.2017.01.018 28143784

2. de Curcio JS, Silva MG, Silva Bailão MG, Báo SN, Casaletti L, Bailão AM, et al. Identification of membrane proteome of. Future Sci OA. 2017;3(4):FSO232.

3. Failla ML. Trace elements and host defense: recent advances and continuing challenges. J Nutr. 2003;133(5 Suppl 1):1443S–7S. doi: 10.1093/jn/133.5.1443S 12730439

4. Bailão EF, Lima PeS, Silva-Bailão MG, Bailão AM, Fernandes GaR, Kosman DJ, et al. Paracoccidioides spp. ferrous and ferric iron assimilation pathways. Front Microbiol. 2015;6:821. doi: 10.3389/fmicb.2015.00821 26441843

5. Fang Z, Sampson SL, Warren RM, Gey van Pittius NC, Newton-Foot M. Iron acquisition strategies in mycobacteria.Tuberc. (Edinb). 2015;95(2):123–30.

6. Ratledge C. Iron Metabolism and Infection. Food Nutr Bull. 2007;28(4_suppl4):S515–S23

7. Gupta KB, Gupta R, Atreja A, Verma M, Vishvkarma S. Tuberculosis and nutrition. Lung India. 2016; 26(1):9.

8. Silva MG, Schrank A, Bailão EFL, Bailão AM, Borges CL, Staats CC, et al. The homeostasis of iron, copper, and zinc in Paracoccidioides brasiliensis, Cryptococcus neoformans var. grubii, and Cryptococcus gattii: a comparative analysis. Front Microbiol. 2011;2:49. doi: 10.3389/fmicb.2011.00049 21833306

9. Camacho E, Niño-Vega GA. Paracoccidioides spp.: Virulence Factors and Immune-Evasion Strategies. Mediators Inflamm. 2017;2017:5313691. doi: 10.1155/2017/5313691 28553014

10. Kiy Y, Machado JM, Mendes RP, Barraviera B, Pereira PCM, Cury PR. Paracoccidioidomycosis in the region of Botucatu (state of São Paulo, Brazil). Evaluation of serum thyroxine (T4) and triiodothyronine (T3) levels and of the response to thyrotropin releasing hormone (TRH). Mycopathologia. 1988;103(1):3–9. doi: 10.1007/bf00437215 3140015

11. Brandão CDG, do Valle ACF, Costa RLB, Wanke B, Tendrich M, Vaisman M. Avaliação funcional da tireóide na paracoccidioidomicose. São Paulo:Moreira Jr. Editora; 2004

12. Chow CC, Mak TWL, Chan CHS, Cockram CS. Euthyroid Sick Syndrome in Pulmonary Tuberculosis before and after Treatment. Ann.Clin.Biochem 1995;32(4):385–91.

13. Barroso CF, Santos LB, Pessoa PP, Vieira DKF, Júnior RMM, Cozzolino SMF, et al. Minerais com função antioxidante e distúrbios da tireóide: avaliação do consumo alimentar em pacientes atendidos em um hospital público de Fortaleza/CE. Nutrire. 2011;36(Suplemento):343-.

14. De Onis M, Blossner M, World Health O. WHO global database on child growth and malnutrition. Geneva: World Health Organization; 1997.

15. Pinheiro ABV, Lacerda EMA, Benzecry EH, GOMES MCS, COSTA VM.Tabela para avaliação de consumo alimentar em medidas caseiras. São Paulo: Atheneu, 2008.

16. Philippi ST.Tabela de composição de alimentos: suporte para decisão nutricional. 5 edição. São Paulo: Manole, 2016.

17. Padovani RM, Amaya-Farfán J, Colugnati FAB, Domene SMA. Dietary reference intakes: aplicabilidade das tabelas em estudos nutricionais. Rev. Nutri. 2006;19(6):741–760.

18. Mendes RP, Cavalcante RdS, Marques SA, Marques MEA, Venturini J, Sylvestre TF, et al. Paracoccidioidomycosis: Current Perspectives from Brazil. Open Microbiol J. 2017;11:224–82. doi: 10.2174/1874285801711010224 29204222

19. Shikanai-Yasuda MA, Telles Filho FdQ, Mendes RP, Colombo AL, Moretti ML. Guideliness in paracoccidioidomycosis. Rev Soc Bras Med Trop. 2006;39(3):297–310. doi: 10.1590/s0037-86822006000300017 16906260

20. Ulbrecht MOO, Gonçalves DA, Zanoni LZG, Nascimento VA. Association Between Selenium and Malondialdehyde as an Efficient Biomarker of Oxidative Stress in Infantile Cardiac Surgery. Biol Trace Elem Res. 2019;187(1):74–79. doi: 10.1007/s12011-018-1378-y 29754283

21. Werneck GL, Hasselmann MH, Gouvêa TG. Panorama dos estudos sobre nutrição e doenças negligenciadas no Brasil. Cien Saude Colet. 2011;16(1):39–62. doi: 10.1590/s1413-81232011000100009 21180814

22. Hildebrand TM, Rosário Filho NA, Telles Filho FdQ, Costa O, Miasaki N, Mira JGS, et al. Paracoccidioidomicose na criança: aspectos clínicos e laboratoriais em 25 casos. J pediatr(Rio J). 1987;63(2):92–7.

23. Fiorillo AM, Takaoka L, Fernandes LAR. Estudo das proteínas séricas na blastomicose americana. Rev Soc Bras Med Trop. 1972;6(3):117–28.

24. Marquez AdS Moreira APV, Leonello PC Nakanishi FA, Itano EN. Serum proteins and fractions, HDL-cholesterol and total IgG and IgE levels in cases of acute and chronic paracoccidioidomycosis. Rev Soc Bras Med Trop. 2009;42(3):245–9. doi: 10.1590/s0037-86822009000300002 19684969

25. dos Santos Nogueira MG, Andrade GMQ, Tonelli E, Diniz SN, Goes AM, Cisalpino PS. Aspectos laboratoriais evolutivos de crianças em tratamento da paracoccidioidomicose. Rev Soc Bras Med Trop. 2006;39:478–83. doi: 10.1590/s0037-86822006000500011 17160327

26. Restrepo A, Restrepo M, de Restrepo F, Aristizábal LH, Moncada LH, Vélez H. Immune responses in paracoccidioidomycosis: A controlled study of 16 patients before and after treatment. J Med Vet Mycol. 1978;16(2):151–63.

27. Sproston NR, Ashworth JJ. Role of C-Reactive Protein at Sites of Inflammation and Infection. Front Immunol.2018;9:754. doi: 10.3389/fimmu.2018.00754 29706967

28. Choi R, Kim H-T, Lim Y, Kim M-J, Kwon OJ, Jeon K, et al. Serum concentrations of trace elements in patients with tuberculosis and its association with treatment outcome. Nutrients. 2015;7(7):5969–81. doi: 10.3390/nu7075263 26197334

29. Moraes ML, Ramalho DM, Delogo KN, Miranda PF, Mesquita ED, de Melo Guedes de Oliveira HM, et al. Association of serum levels of iron, copper, and zinc, and inflammatory markers with bacteriological sputum conversion during tuberculosis treatment. Biol Trace Elem Res. 2014;160(2):176–84. doi: 10.1007/s12011-014-0046-0 24958018

30. Wintergerst ES, Maggini S, Hornig DH. Contribution of Selected Vitamins and Trace Elements to Immune Function. Ann. Nutr. Metab. 2007;51(4):301–23. doi: 10.1159/000107673 17726308

31. Kocyigit A, Erel O, Seyrek A, Gurel M, Aktepe N, Avci S, et al. Effects of antimonial therapy on serum zinc, copper and iron concentrations in patients with cutaneous Leishmaniasis in Turkey. East J Med.1998; 3(2)58–61.

32. Erickson KL, Medina EA, Hubbard NE. Micronutrients and innate immunity. J Infect Dis. 2000;182(Supplement_1):S5–S10.

33. Ciftci TU, Ciftci B, Yis Ö, Guney Y, Bilgihan A, Ogretensoy M. Changes in serum selenium, copper, zinc levels and Cu/Zn ratio in patients with pulmonary tuberculosis during therapy. Biol Trace Elem Res. 2003;95(1):65–71. doi: 10.1385/BTER:95:1:65 14555800

34. Libardo MDJ, de la Fuente-Nuñez C, Anand K, Krishnamoorthy G, Kaiser P, Pringle SC, et al. Phagosomal Copper-Promoted Oxidative Attack on Intracellular Mycobacterium tuberculosis. ACS Infect Dis. 2018;4(11):1623–34. doi: 10.1021/acsinfecdis.8b00171 30141623

35. Deigendesch N, Zychlinsky A, Meissner F. Copper Regulates the Canonical NLRP3 Inflammasome. J. Immunol. 2018:ji1700712.

36. Calvi SA, Soares AMVC, Peraçoli MTS, Franco M, Ruiz RL Jr, Marcondes-Machado J, et al. Study of bronchoalveolar lavage fluid in paracoccidioidomycosis: cytopathology and alveolar macrophage function in response to gamma interferon; comparison with blood monocytes. Microbes Infect. 2003;5(15):1373–9. doi: 10.1016/j.micinf.2003.05.001 14670450

37. Venturini J, Cavalcante RS, de Assis Golim M, Marchetti CM, de Azevedo PZ, Amorim BC, et al. Phenotypic and functional evaluations of peripheral blood monocytes from chronic-form paracoccidioidomycosis patients before and after treatment.BMC Infect. Dis. 2014;14(1):552.

38. Cozzolino SMF. Mineral deficiencies. Estudos avançados. 2007;21(60):119–26.

39. Fietz VR. Estado nutricional, consumo de alimentos e condições socioeconômicas das famílias de assentamento rural em Mato Grosso do Sul, Brasil. 2007.

40. Pourfallah F, Javadian S, Zamani Z, Saghiri R, Sadeghi S, Zarea B, et al. Evaluation of serum levels of essential trace elements in patients with pulmonary tuberculosis before and after treatment by age and gender. Pak J Biol Sci. 2011;14(10):590–4. doi: 10.3923/pjbs.2011.590.594 22097095

41. Lal CS, Kumar S, Ranjan A, Rabidas VN, Verma N, Pandey K, et al. Comparative analysis of serum zinc, copper, magnesium, calcium and iron level in acute and chronic patients of visceral leishmaniasis. J Trace Elem Med Biol. 2013;27(2):98–102. doi: 10.1016/j.jtemb.2012.09.007 23199594

42. Gammoh NZ, Rink L. Zinc in Infection and Inflammation. Nutrients. 2017;9(6):624.

43. Jarosz M, Olbert M, Wyszogrodzka G, Młyniec K, Librowski T. Antioxidant and anti-inflammatory effects of zinc. Zinc-dependent NF-κB signaling. Inflammopharmacology. 2017;25(1):11–24. doi: 10.1007/s10787-017-0309-4 28083748

44. Vignesh KS, Figueroa JAL, Porollo A, Caruso JA, Deepe GS Jr. Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. Immunity. 2013;39(4):697–710. doi: 10.1016/j.immuni.2013.09.006 24138881

45. Botella H, Stadthagen G, Lugo-Villarino G, de Chastellier C, Neyrolles O. Metallobiology of host—pathogen interactions: an intoxicating new insight. Trends Microbiol. 2012;20(3):106–12. doi: 10.1016/j.tim.2012.01.005 22305804

46. Malafaia G. Captação de ferro pelos parasitos do gênero Leishmania. Rev. biocienc.2008;14(1).

47. Bricks LF. Ferro e infecções: atualização. Pediatria (Säo Paulo). 1994;16(1):34–43.

48. Cash JM, Sears DA. The anemia of chronic disease: spectrum of associated diseases in a series of unselected hospitalized patients. Am J Med. 1989;87(6):638–44. doi: 10.1016/s0002-9343(89)80396-1 2589399

49. de Macêdo ÉMC, Amorim MAF, da Silva ACS, de Castro CMMB. Efeitos da deficiência de cobre, zinco e magnésio sobre o sistema imune de crianças com desnutrição grave. Rev Paul Pediatr. 2010;28(3):329–36.

50. Murray HW, Nathan CF. Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. J Exp Med. 1999;189(4):741–6. doi: 10.1084/jem.189.4.741 9989990

51. Tomkins A. Assessing Micronutrient Status in the Presence of Inflammation. J Nutr. 2003;133(5):1649S–55S.

52. Kassu A, Yabutani T, Mahmud ZH, Mohammad A, Nguyen N, Huong BT, et al. Alterations in serum levels of trace elements in tuberculosis and HIV infections. Eur J Clin Nutr. 2006;60(5):580–6. doi: 10.1038/sj.ejcn.1602352 16340948

53. Morreale de Escobar G, Pastor R, Obregon MJ, Escobar del Rey F. Effects of maternal thyroidectomy on rat embryonic T4 and T3 contents and development, before and after onset of fetal thyroid function. frontiers of thyroidology.Plenum Medical. 1986:1177–81.

54. Matarazzo P, Palomba E, Lala R, Ciuti E, Altare F, Sanctis Ld, et al. Growth impairment, IGF I hyposecretion and thyroid dysfunction in children with perinatal HIV‐1 infection. Acta Paediatr. 1994;83(10):1029–34. doi: 10.1111/j.1651-2227.1994.tb12977.x 7841697

55. Chiarelli F, Verrotti A, Galli L, Basciani F, De Martino M. Endocrine dysfunction in children with HIV-1 infection. J Pediatr Endocrinol Metab. 1999;12(1):17–26. doi: 10.1515/jpem.1999.12.1.17 10392344

56. Fundaro C, Olivieri A, Rendeli C, Genovese O, Martino AM, D’Archivio M, et al. Occurrence of anti-thyroid autoantibodies in children vertically infected with HIV-1. J Pediatr Endocrinol Metab. 1998;11(6):745–50. doi: 10.1515/jpem.1998.11.6.745 9829230

57. Boelen A, Kwakkel J, Platvoet-ter Schiphorst M, Mentrup B, Baur A, Koehrle, et al. Interleukin-18, a proinflammatory cytokine, contributes to the pathogenesis of non-thyroidal illness mainly via the central part of the hypothalamus-pituitary-thyroid axis. Eur J Endocrinol. 2004;151(4): 497–502. doi: 10.1530/eje.0.1510497 15476451

58. Fabris LR, Andrade ÚV, Santos AFD, Marques APDC, Oliveira SMDVL, Mendes RP. Decreasing prevalence of the acute/subacute clinical form of paracoccidioidomycosis in Mato Grosso do Sul State, Brazil. Rev Inst Med trop S Paulo. 2014; 56(2): 121–125. doi: 10.1590/S0036-46652014000200006 24626413

59. Jain RB. Thyroid function and serum copper, selenium, and zinc in general US population. Biol Trace Elem Res. 2014;159(1–3):87–98. doi: 10.1007/s12011-014-9992-9 24789479

60. Northrop-Clewes CA, Thurnham DI. Monitoring micronutrients in cigarette smokers. Clin Chim Acta. 2007;377(1–2): 14–38. doi: 10.1016/j.cca.2006.08.028 17045981

Dynamics of plasma micronutrient concentrations and their correlation with serum proteins and thyroid hormones in patients with paracoccidioidomycosis

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