European Journal of Nutrition

, Volume 53, Issue 1, pp 73–82 | Cite as

Ilex paraguariensis (yerba mate) improves endocrine and metabolic disorders in obese rats primed by early weaning

  • Natália da S. Lima
  • Juliana G. Franco
  • Nayara Peixoto-Silva
  • Lígia A. Maia
  • Andrea Kaezer
  • Israel Felzenszwalb
  • Elaine de Oliveira
  • Egberto G. de Moura
  • Patricia Cristina LisboaEmail author
Original Contribution



We showed that early weaned rats developed obesity, hyperleptinemia, leptin and insulin resistance at adulthood. Here, we studied the potential beneficial effects of Ilex paraguariensis aqueous solution upon body composition, glycemia, lipid and hormonal profiles, leptin signaling and NPY content.


To induce early weaning, lactating rats’ teats were blocked with a bandage to interrupt lactation during the last 3 days (EW group), while control offspring had free access to milk throughout lactation (C group). In postnatal day (PN) 150, EW offspring were subdivided into: EW and EW+ mate groups treated, respectively, with water or yerba mate aqueous solution (1 g/kg BW/day, gavage) during 30 days. C offspring received water for gavage. In PN180, offspring were killed.


EW+ mate group presented lower body weight (−10 %), adipose mass (retroperitoneal:−40 % and epididymal:−44 %), total body fat (−43 %), subcutaneous fat (−46 %), visceral adipocyte area (−21 %), triglyceridemia (−31 %) and hypothalamic NPY content (−37 %) compared to EW group. However, hyperglycemia and lower HDL-c levels observed in EW group were not reverted with mate treatment. Although the hyperleptinemia, lower hypothalamic JAK2 and pSTAT3 content of EW group were not corrected by mate treatment, the hyperphagia and higher hypothalamic SOCS-3 content were normalized in EW+ mate group, indicating that the central leptin resistance could be restored.


Thus, the therapy with yerba mate solution was capable to reverse abdominal obesity, leptin resistance and hypertriglyceridemia, suggesting an important role of this bioactive component in the management of obesity in this programming model.


Obesity Programming Fat mass Leptin Ilex paraguariensis 



All authors are grateful to Miss Monica Moura and Mr. Ulisses Risso Siqueira for technical assistance as well as to Mr. José Firmino Nogueira Neto for lipid profile analysis (LabLip – State University of Rio de Janeiro). NS Lima, JG Franco and LA Maia participated in collection, analysis and interpretation of data. A Kaezer and I Felzenszwalb were responsible for mate treatment; N Peixoto-Silva was responsible for adipocyte morphometry; EG Moura, E Oliveira and PC Lisboa were responsible for conception and design, and also performed drafting and critical revising of the manuscript. This research was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (National Council for Scientific and Technological Development), Coordenacão de Aperfeiçoamento de Pessoal de Nível Superior—CAPES (Coordination for the Enhancement of Higher Education Personnel) and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro—FAPERJ (Carlos Chagas Filho Research Foundation of the State of Rio de Janeiro).

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.


  1. 1.
    US Department of Health and Human Services, Centers for Disease Control and Prevention (2007) Physical activity and good nutrition: essential elements to prevent chronic diseases and obesity. Available from: (cited 6 December 2007)
  2. 2.
    Barker DJ (2003) The developmental origins of adult disease. Eur J Epidemiol 18:733–736CrossRefGoogle Scholar
  3. 3.
    Moura EG, Lisboa PC, Passos MC (2008) Neonatal programming of neuroimmunomodulation-role of adipocytokines and neuropeptides. NeuroImmunoModulation 15(3):176–188CrossRefGoogle Scholar
  4. 4.
    Gluckman PD, Hanson MA (2007) Developmental plasticity and human disease: research directions. J Intern Med 261(5):461–471CrossRefGoogle Scholar
  5. 5.
    Bonomo IT, Lisboa PC, Pereira AR, Passos MC, Moura EG (2007) Prolactin inhibition in dams during lactation programs for overweight and leptin resistance in adult offspring. J Endocrinol 192:339–344CrossRefGoogle Scholar
  6. 6.
    Moura EG, Bonomo IT, Nogueira-Neto JF, de Oliveira E, Trevenzoli IH, Reis AM, Passos MC, Lisboa PC (2009) Maternal prolactin inhibition during lactation programs for metabolic syndrome in adult progeny. J Physiol 15:4919–4929CrossRefGoogle Scholar
  7. 7.
    Bonomo IT, Lisboa PC, Passos MC, Alves SB, Reis AM, de Moura EG (2008) Prolactin inhibition at the end of lactation programs for a central hypothyroidism in adult rat. J Endocrinol 198:331–337CrossRefGoogle Scholar
  8. 8.
    Lima NS, de Moura EG, Passos MC, Nogueira Neto FJ, Reis AM, de Oliveira E, Lisboa PC (2011) Early weaning causes undernutrition for a short period and programmes some metabolic syndrome components and leptin resistance in adult rat offspring. Br J Nutr 105(9):1405–1413CrossRefGoogle Scholar
  9. 9.
    Bastos DHM, De Oliveira DM, Matsumoto RLT, Carvalho PO, Ribeiro ML (2007) Yerba mate: pharmacological properties, research and biotechnology. Med Aromat Plant Sci Biotechnol 1:37–46Google Scholar
  10. 10.
    Heck CI, de Mejia EG (2007) Yerba Mate Tea (Ilex paraguariensis): a comprehensive review on chemistry, health implications, and technological considerations. J Food Sci 72(9):138–151CrossRefGoogle Scholar
  11. 11.
    Miranda DD, Arcari DP, Pedrazzoli J, de Carvalho PO, Cerutti SM, Bastos DH, Ribeiro ML (2008) Protective effects of mate tea (Ilex paraguariensis) on H2O2-induced DNA damage and DNA repair in mice. Mutagenesis 23:261–265CrossRefGoogle Scholar
  12. 12.
    Arçari DP, Bartchewsky W, dos Santos TW, Oliveira KA, Funck A, Pedrazzoli J, de Souza MF, Saad MJ, Bastos DH, Gambero A, de Carvalho PO, Ribeiro ML (2009) Antiobesity effects of yerba maté extract (Ilex paraguariensis) in high-fat diet-induced obese mice. Obesity 17(12):2127–2133CrossRefGoogle Scholar
  13. 13.
    Arçari DP, Bartchewsky W Jr, dos Santos TW, Oliveira KA, De Oliveira CC, Gotardo ÉM, Pedrazzoli J Jr, Gambero A, Ferraz LF, de Carvalho PO, Ribeiro ML (2011) Anti-inflammatory effects of yerba maté extract (Ilex paraguariensis) ameliorate insulin resistance in mice with high fat diet-induced obesity. Mol Cell Endocrinol 335(2):110–115CrossRefGoogle Scholar
  14. 14.
    Pang J, Choi Y, Park T (2008) Ilex paraguariensis extract ameliorates obesity induced by high-fat diet: potential role of AMPK in the visceral adipose tissue. Arch Biochem Biophys 476:178–185CrossRefGoogle Scholar
  15. 15.
    Kang YR, Lee HY, Kim JH, Moon DI, Seo MY, Park SH, Choi KH, Kim CR, Kim SH, Oh JH, Cho SW, Kim SY, Kim MG, Chae SW, Kim O, Oh HG (2012) Anti-obesity and anti-diabetic effects of Yerba Mate (Ilex paraguariensis) in C57BL/6J mice fed a high-fat diet. Lab Anim Res 28(1):23–29CrossRefGoogle Scholar
  16. 16.
    Boaventura BC, Di Pietro PF, Stefanuto A, Klein GA, de Morais EC, de Andrade F, Wazlawik E, da Silva EL (2012) Association of mate tea (Ilex paraguariensis) intake and dietary intervention and effects on oxidative stress biomarkers of dyslipidemic subjects. Nutrition 28(6):657–664CrossRefGoogle Scholar
  17. 17.
    Oliveira DM, Freitas HS, Souza MF, Arçari DP, Ribeiro ML, Carvalho PO, Bastos DH (2008) Yerba Maté (Ilex paraguariensis) aqueous extract decreases intestinal SGLT1 gene expression but does not affect other biochemical parameters in alloxan-diabetic Wistar rats. J Agric Food Chem 26; 56(22):10527–10532Google Scholar
  18. 18.
    Miranda DD, Arçari DP, Pedrazzoli J Jr, de Carvalho PO, Cerutti SM, Bastos DH, Ribeiro ML (2008) Protective effects of mate tea (Ilex paraguariensis) on H2O2-induced DNA damage and DNA repair in mice. Mutagenesis 23(4):261–265CrossRefGoogle Scholar
  19. 19.
    Kaezer AR, Aiub CAF, Mazzei JL, Ribeiro-Pintob LF, Felzenszwalb I (2012) Antimutagenic effect and phenolic content of green and roasted yerba mate beverages in different packages available in the Brazilian market. CyTA J Food 144–151. doi: 10.1080/19476337.2011.601429
  20. 20.
    Andrade F, de Albuquerque CA, Maraschin M, da Silva EL (2012) Safety assessment of yerba mate (Ilex paraguariensis) dried extract: results of acute and 90 days subchronic toxicity studies in rats and rabbits. Food Chem Toxicol 50(2):328–334CrossRefGoogle Scholar
  21. 21.
    Fagundes AT, Moura EG, Passos MC, Oliveira E, Toste FP, Bonomo IT, Trevenzoli IH, Garcia RM, Lisboa PC (2007) Maternal low-protein diet during lactation programmes body composition and glucose homeostasis in the adult rat offspring. Br J Nutr 98:922–928CrossRefGoogle Scholar
  22. 22.
    Lowry OH, Rosebrough NJ, Farr AL, Randal LRJ (1951) Protein measuremente with the folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  23. 23.
    Younes-Rapozo V, Moura EG, Lima NS, Barradas PC, Manhães AC, Oliveira E, Lisboa PC (2012) Early weaning is associated with higher neuropeptide Y (NPY) and lower cocaine- and amphetamine-regulated transcript (CART) expressions in the paraventricular nucleus (PVN) in adulthood. Br J Nutr. doi: 10.1017/S0007114512000487
  24. 24.
    Mosimann ALP, Wilhelm-Filho D, Silva EL (2006) Aqueous extract of Ilex paraguariensis attenuates the progression of atherosclerosis in cholesterol.fed rabbits. BioFactors 23:1–12Google Scholar
  25. 25.
    Rodriguez de Sotillo DV, Hadley M (2002) Chlorogenic acid modifies plasma and liver concentrations of: cholesterol, triacylglycerol, and minerals in (fa/fa) Zucker rats. J Nutr Biochem 13:717–726CrossRefGoogle Scholar
  26. 26.
    Hussein GM, Matsuda H, Nakamura S, Hamao M, Akiyama T, Tamura K, Yoshikawa M (2011) Mate tea (Ilex paraguariensis) promotes satiety and body weight lowering in mice: involvement of glucagon-like peptide-1. Biol Pharm Bull 34(12):1849–1855CrossRefGoogle Scholar
  27. 27.
    Velloso LA, Schwartz MW (2011) Altered hypothalamic function in diet-induced obesity. Int J Obes (Lond) 35(12):1455–1465. doi: 10.1038/ijo.2011.56 CrossRefGoogle Scholar
  28. 28.
    Zabolotny JM, Bence-Hanulec KK, Stricker-Krongrad A, Haj F, Wang Y, Minokoshi Y, KimYB, Elmquist JK, Tartaglia LA, Kahn BB et al (2002) PTP1B regulates leptin signal transduction in vivo. Developmental Cell 2:489–495Google Scholar
  29. 29.
    Billington CJ, Briggs JE, Harker S, Grace M, Levine AS (1994) Neuropeptide Y in hypothalamic paraventricular nucleus: a center coordinating energy metabolism. Am J Physiol 266:1765–1770Google Scholar
  30. 30.
    Seo S, Ju S, Chung H, Lee D, Park S (2008) Acute effects of glucagon-like peptide-1 on hypothalamic neuropeptide and AMP activated kinase expression in fasted rats. Endocr J 55(5):867–874CrossRefGoogle Scholar
  31. 31.
    Köhnke R, Lindqvist A, Göransson N, Emek SC, Albertsson PA, Rehfeld JF, Hultgårdh-Nilsson A, Erlanson-Albertsson C (2009) Thylakoids suppress appetite by increasing cholecystokinin resulting in lower food intake and body weight in high-fat fed mice. Phytother Res 23(12):1778–1783CrossRefGoogle Scholar
  32. 32.
    Albertsson PA, Köhnke R, Emek SC, Mei J, Rehfeld JF, Akerlund HE, Erlanson-Albertsson C (2007) Chloroplast membranes retard fat digestion and induce satiety: effect of biological membranes on pancreatic lipase/co-lipase. Biochem J 401:727–733CrossRefGoogle Scholar
  33. 33.
    Yudkin JS, Stehouwer CD, Emeis JJ, Coppack SW (1999) C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 19:972–978CrossRefGoogle Scholar
  34. 34.
    Zhang X, Zhang G, Zhang H, Karin M, Bai H, Cai D (2008) Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 135:61–73CrossRefGoogle Scholar
  35. 35.
    Costa-e-Sousa RH, Souza LL, Calviño C, Cabanelas A, Almeida NA, Oliveira KJ, Pazos-Moura CC (2011) Central NPY-Y5 receptors activation plays a major role in fasting-induced pituitary-thyroid axis suppression in adult rat. Regul Pept 171(1–3):43–47. doi: 10.1016/j.regpep.2011.07.001 CrossRefGoogle Scholar
  36. 36.
    Lima NS, Moura EG, Franco JG, Pinheiro CR, Pazos-Moura CC, Cabanelas A, Carlos AS, Nascimento-Saba CC, de Oliveira E, Lisboa PC (2013) Developmental plasticity of endocrine disorders in obesity model primed by early weaning in dams. Horm Metab Res 45:22–30Google Scholar
  37. 37.
    Pimentel GD, Lira FS, Rosa JC, Caris AV, Pinheiro F, Ribeiro EB, Oller do Nascimento CM, Oyama LM (2012) Yerba mate extract (Ilex paraguariensis) attenuates both central and peripheral inflammatory effects of diet-induced obesity in rats. J Nutr Biochem. doi: 10.1016/j.jnutbio.2012.04.016
  38. 38.
    Hussein GM, Matsuda H, Nakamura S, Akiyama T, Tamura K, Yoshikawa M (2011) Protective and ameliorative effects of maté (Ilex paraguariensis) on metabolic syndrome in TSOD mice. Phytomedicine 19(1):88–97. doi: 10.1016/j.phymed.2011.06.036 CrossRefGoogle Scholar
  39. 39.
    Paz-Filho GJ, Volaco A, Suplicy HL, Radominski RB, Boguszewski CL (2009) Decrease in leptin production by the adipose tissue in obesity associated with severe metabolic syndrome. Arq Bras Endocrinol Metabol 53(9):1088–1095CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Natália da S. Lima
    • 1
  • Juliana G. Franco
    • 1
  • Nayara Peixoto-Silva
    • 1
  • Lígia A. Maia
    • 1
  • Andrea Kaezer
    • 1
    • 2
  • Israel Felzenszwalb
    • 2
  • Elaine de Oliveira
    • 1
  • Egberto G. de Moura
    • 1
  • Patricia Cristina Lisboa
    • 1
    • 3
    Email author
  1. 1.Laboratory of Endocrine Physiology, Department of Physiological Sciences, Roberto Alcantara Gomes Biology InstituteState University of Rio de JaneiroRio de JaneiroBrazil
  2. 2.Department of Biophysics and Biometry, Roberto Alcantara Gomes Biology InstituteState University of Rio de JaneiroRio de JaneiroBrazil
  3. 3.Departamento de Ciências Fisiológicas, 5° andar, Instituto de BiologiaUniversidade do Estado do Rio de JaneiroRio de JaneiroBrazil

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