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Nutrition in acute and chronic diseases

Effect of parathyroidectomy on bone tissue biomarkers and body composition in patients with chronic kidney disease and secondary hyperparathyroidism

European Journal of Clinical Nutrition volume 75, pages 1126–1133 (2021)Cite this article

Subjects

Abstract

Background/objective

Loss of renal function may induce secondary hyperparathyroidism (s-HPT), which triggers several complications leading to an extreme decline in quality of life and increased mortality in affected patients. We evaluated whether parathyroidectomy (PTx), as surgical treatment for s-HPT, modifies body composition, and hormones involved in the protein-energy metabolism of affected patients.

Subjects/methods

Overall, 30 s-HPT patients were evaluated at two times, before PTx (pre PTx) and 6 months after PTx (post PTx). Patients were evaluated by biochemistry analysis, anthropometry, electrical bioimpedance (BIA), food intake diary, handgrip strength, and modified global subjective nutritional assessment (SGA).

Results

After PTx, patients showed decreased serum levels of total and ionic calcium, as well as decreased alkaline phosphatase and PTH, and increased 25 (OH) vitamin D. These results demonstrate that PTx was efficient to correct part of the mineral disorder. We also observed an increase in caloric intake, body weight, body mass index (BMI), phase angle, handgrip strength, SGA score, and a decreasing in the percentage of weight loss. The osteocalcin concentration of both carboxylated (cOC) and undercarboxylated form was diminished post PTx. The cOC correlated with bone metabolism markers and SGA score.

Conclusions

PTx modified body composition improving nutritional status and preventing the progression of weight loss with increased of energy intake, BMI, handgrip strength, phase angle of BIA, and SGA score. The present study also suggests an association of cOC with bone markers and SGA score. Further studies are needed to better clarify these associations with larger sample size.

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Fig. 1: Weight loss assessment and nutritional status of pre- and post-PTx patients were analyzed by anthropometry and subjective global assessment (SGA), respectively.

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References

  1. Slatopolsky E. The intact nephron hypothesis: the concept and its implications for phosphate management in CKD-related mineral and bone disorder. Kidney Int. 2011;79121:S3–8.

    PubMed  Google Scholar 

  2. Custódio MR, Canziani ME, Moysés RM, Barreto FC, Neves CL, de Oliveira RB, et al. Clinical protocol and therapeutic guidelines for the treatment of secondary hyperparathyroidism in patients with chronic kidney disease. J Bras Nefrol. 2013;35:308–22.

    PubMed  Google Scholar 

  3. Barreto FC, Bucharles SGE. Predicting the successfulness of parathyroidectomy: new lessons from an old challenge. J Bras Nefrol. 2017;39:100–1.

    PubMed  Google Scholar 

  4. Sampaio EeA, Moysés RM, Nefrologia SBD. Parathyroidectomy in CKD. J Bras Nefrol. 2011;33:221–4.

    Google Scholar 

  5. Oliveira RB, Silva EN, Charpinel DM, Gueiros JE, Neves CL, Sampaio EEA, et al. Secondary hyperparathyroidism status in Brazil: Brazilian census of parathyroidectomy. J Bras Nefrol. 2011;33:457–62.

    PubMed  Google Scholar 

  6. Araújo IC, Kamimura MA, Draibe SA, Canziani ME, Manfredi SR, Avesani CM, et al. Nutritional parameters and mortality in incident hemodialysis patients. J Ren Nutr. 2006;16:27–35.

    PubMed  Google Scholar 

  7. Vegine PM, Fernandes AC, Torres MR, Silva MI, Avesani CM. Assessment of methods to identify protein-energy wasting in patients on hemodialysis. J Bras Nefrol. 2011;33:55–61.

    PubMed  Google Scholar 

  8. Pérez-Torres A, González Garcia ME, San José-Valiente B, Bajo Rubio MA, Celadilla Diez O, López-Sobaler AM, et al. Protein-energy wasting syndrome in advanced chronic kidney disease: prevalence and specific clinical characteristics. Nefrologia 2018;38:141–51.

    PubMed  Google Scholar 

  9. Lee YJ, Cho S, Kim SR. The association between serum adiponectin levels and nutritional status of hemodialysis patients. Ren Fail. 2011;33:506–11.

    CAS  PubMed  Google Scholar 

  10. Pittas AG, Harris SS, Eliades M, Stark P, Dawson-Hughes B. Association between serum osteocalcin and markers of metabolic phenotype. J Clin Endocrinol Metab. 2009;94:827–32.

    CAS  PubMed  Google Scholar 

  11. Jia T, Carrero JJ, Lindholm B, Stenvinkel P. The complex role of adiponectin in chronic kidney disease. Biochimie 2012;94:2150–6.

    CAS  PubMed  Google Scholar 

  12. Kindblom JM, Ohlsson C, Ljunggren O, Karlsson MK, Tivesten A, Smith U, et al. Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Min Res. 2009;24:785–91.

    CAS  Google Scholar 

  13. Kalantar-Zadeh K, Kleiner M, Dunne E, Lee GH, Luft FC. A modified quantitative subjective global assessment of nutrition for dialysis patients. Nephrol Dial Transpl. 1999;14:1732–8.

    CAS  Google Scholar 

  14. Kalantar-Zadeh K, Kopple JD, Block G, Humphreys MH. A malnutrition-inflammation score is correlated with morbidity and mortality in maintenance hemodialysis patients. Am J Kidney Dis. 2001;38:1251–63.

    CAS  PubMed  Google Scholar 

  15. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep. Ser. 2000;894:i–xii. 1-253

    Google Scholar 

  16. Clinical practice guidelines for nutrition in chronic renal failure. K/DOQI, National Kidney Foundation. Am J Kidney Dis. 2000;35:S1–140.

    Google Scholar 

  17. Frisancho AR. New norms of upper limb fat and muscle areas for assessment of nutritional status. Am J Clin Nutr. 1981;34:2540–5.

    CAS  PubMed  Google Scholar 

  18. Chumlea WC, Roche AF, Steinbaugh ML. Estimating stature from knee height for persons 60 to 90 years of age. J Am Geriatr Soc. 1985;33:116–20.

    CAS  PubMed  Google Scholar 

  19. Leal VO, Stockler-Pinto MB, Farage NE, Aranha LN, Fouque D, Anjos LA, et al. Handgrip strength and its dialysis determinants in hemodialysis patients. Nutrition. 2011;27:1125–9.

    PubMed  Google Scholar 

  20. Pecoits-Filho R, Lindholm B, Stenvinkel P. The malnutrition, inflammation, and atherosclerosis (MIA) syndrome - the heart of the matter. Nephrol Dial Transpl. 2002;17:28–31.

    CAS  Google Scholar 

  21. Mafra D, Guebre-Egziabher F, Fouque D. Body mass index, muscle and fat in chronic kidney disease: questions about survival. Nephrol Dial Transpl. 2008;23:2461–6.

    CAS  Google Scholar 

  22. Peters BS, Moyses RM, Jorgetti V, Martini LA. Effects of parathyroidectomy on bone remodeling markers and vitamin D status in patients with chronic kidney disease-mineral and bone disorder. Int Urol Nephrol. 2007;39:1251–6.

    CAS  PubMed  Google Scholar 

  23. Wapensky T, Alexander SR, Sarwal M. Postdialysis albumin: a better nutrition marker in pediatric hemodialysis patients? J Ren Nutr. 2004;14:45–51.

    PubMed  Google Scholar 

  24. Yeun JY, Kaysen GA. Factors influencing serum albumin in dialysis patients. Am J Kidney Dis. 1998;32:S118–25.

    CAS  PubMed  Google Scholar 

  25. Jones CH, Akbani H, Croft DC, Worth DP. The relationship between serum albumin and hydration status in hemodialysis patients. J Ren Nutr. 2002;12:209–12.

    PubMed  Google Scholar 

  26. Jones CH, Wolfenden RC, Wells LM. Is subjective global assessment a reliable measure of nutritional status in hemodialysis? J Ren Nutr. 2004;14:26–30.

    PubMed  Google Scholar 

  27. Grunfeld C, Zhao C, Fuller J, Pollack A, Moser A, Friedman J, et al. Endotoxin and cytokines induce expression of leptin, the ob gene product, in hamsters. J Clin Invest. 1996;97:2152–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Nakanishi I, Moutabarrik A, Okada N, Kitamura E, Hayashi A, Syouji T, et al. Interleukin-8 in chronic renal failure and dialysis patients. Nephrol Dial Transpl. 1994;9:1435–42.

    CAS  Google Scholar 

  29. Lindholm B, Heimbürger O, Stenvinkel P. What are the causes of protein-energy malnutrition in chronic renal insufficiency? Am J Kidney Dis. 2002;39:422–5.

    PubMed  Google Scholar 

  30. Stenvinkel P, Lindholm B, Heimbürger M, Heimbürger O. Elevated serum levels of soluble adhesion molecules predict death in pre-dialysis patients: association with malnutrition, inflammation, and cardiovascular disease. Nephrol Dial Transpl. 2000;15:1624–30.

    CAS  Google Scholar 

  31. Chen C, Wu H, Zhong L, Wang X, Xing ZJ, Gao BH. Impacts of parathyroidectomy on renal anemia and nutritional status of hemodialysis patients with secondary hyperparathyroidism. Int J Clin Exp Med. 2015;8:9830–8.

    PubMed  PubMed Central  Google Scholar 

  32. Ribeiro MCCB, Vogt BP, Vannini FCD, Caramori JCT. Role of parathyroid hormone in anorexia on maintenance hemodialysis patients. Clin Nutr ESPEN. 2019;34:137–41.

    PubMed  Google Scholar 

  33. Kir S, Komaba H, Garcia AP, Economopoulos KP, Liu W, Lanske B, et al. PTH/PTHrP receptor mediates cachexia in models of kidney failure and cancer. Cell Metab. 2016;23:315–23.

    CAS  PubMed  Google Scholar 

  34. Rayner HC, Stroud DB, Salamon KM, Strauss BJ, Thomson NM, Atkins RC, et al. Anthropometry underestimates body protein depletion in haemodialysis patients. Nephron. 1991;59:33–40.

    CAS  PubMed  Google Scholar 

  35. Segall L, Mardare NG, Ungureanu S, Busuioc M, Nistor I, Enache R, et al. Nutritional status evaluation and survival in haemodialysis patients in one centre from Romania. Nephrol Dial Transpl. 2009;24:2536–40.

    Google Scholar 

  36. Bansal N, Zelnick LR, Himmelfarb J, Chertow GM. Bioelectrical impedance analysis measures and clinical outcomes in CKD. Am J Kidney Dis. 2018;72:662–72.

    PubMed  Google Scholar 

  37. Beberashvili I, Azar A, Sinuani I, Shapiro G, Feldman L, Stav K, et al. Bioimpedance phase angle predicts muscle function, quality of life and clinical outcome in maintenance hemodialysis patients. Eur J Clin Nutr. 2014;68:683–9.

    CAS  PubMed  Google Scholar 

  38. Lu JL, Kalantar-Zadeh K, Ma JZ, Quarles LD, Kovesdy CP. Association of body mass index with outcomes in patients with CKD. J Am Soc Nephrol. 2014;25:2088–96.

    PubMed  PubMed Central  Google Scholar 

  39. Hung SC, Lai YS, Kuo KL, Tarng DC. Volume overload and adverse outcomes in chronic kidney disease: clinical observational and animal studies. J Am Heart Assoc. 2015;4:e001918.

  40. Stenvinkel P, Gillespie IA, Tunks J, Addison J, Kronenberg F, Drueke TB, et al. Inflammation modifies the paradoxical association between body mass index and mortality in hemodialysis patients. J Am Soc Nephrol. 2016;27:1479–86.

    CAS  PubMed  Google Scholar 

  41. Rodríguez-Carmona A, Pérez Fontán M, Cordido F, García Falcón T, García-Buela J. Hyperleptinemia is not correlated with markers of protein malnutrition in chronic renal failure. A cross-sectional study in predialysis, peritoneal dialysis and hemodialysis patients. Nephron. 2000;86:274–80.

    PubMed  Google Scholar 

  42. Bossola M, Muscaritoli M, Valenza V, Panocchia N, Tazza L, Cascino A, et al. Anorexia and serum leptin levels in hemodialysis patients. Nephron Clin Pr. 2004;97:c76–82.

    CAS  Google Scholar 

  43. Scholze A, Rattensperger D, Zidek W, Tepel M. Low serum leptin predicts mortality in patients with chronic kidney disease stage 5. Obesity. 2007;15:1617–22.

    CAS  PubMed  Google Scholar 

  44. Kara E, Ahbap E, Sahutoglu T, Sakaci T, Basturk T, Koc Y, et al. Elevated serum leptin levels are associated with good nutritional status in non-obese chronic hemodialysis patients. Clin Nephrol. 2015;83:147–53.

    CAS  PubMed  Google Scholar 

  45. Nanayakkara PW, Le Poole CY, Fouque D, van Guldener C, Stehouwer CD, Smulders YM, et al. Plasma adiponectin concentration has an inverse and a non linear association with estimated glomerular filtration rate in patients with K/DOQI 3 - 5 chronic kidney disease. Clin Nephrol. 2009;72:21–30.

    CAS  PubMed  Google Scholar 

  46. Hryszko T, Brzosko S, Rydzewska-Rosołowska A, Koc-Żórawska E, Naumnik B, Myśliwiec M. Effect of secondary hyperparathyroidism treatment with cinacalcet on selected adipokines and markers of endothelial injury in hemodialysis patients: a preliminary report. Pol Arch Med Wewn. 2012;122:148–53.

    CAS  PubMed  Google Scholar 

  47. Csiky B, Sági B, Peti A, Lakatos O, Prémusz V, Sulyok E. The impact of osteocalcin, osteoprotegerin and osteopontin on arterial stiffness in chronic renal failure patients on hemodialysis. Kidney Blood Press Res. 2017;42:1312–21.

    CAS  PubMed  Google Scholar 

  48. Roumeliotis S, Dounousi E, Eleftheriadis T, Liakopoulos V. Association of the inactive circulating matrix Gla protein with vitamin K intake, calcification, mortality, and cardiovascular disease: a review. Int J Mol Sci. 2019;20:628.

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Acknowledgements

The authors wish to acknowledge Rackel Mota da Costa for their active participation during the data collection.

Funding

This study was supported by grants from the Fundação de Amparo à Pesquisa do Estado de São Paulo (São Paulo State Research Foundation—grant number 2015/13126-8).

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Authors and Affiliations

  1. LIM 16 - Laboratorio de Fisiopatologia Renal, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de Sao Paulo, Sao Paulo, Brasil

    Flavia Ramos de Siqueira, Karin Carneiro de Oliveira, Wagner Vasques Dominguez, César Augusto Madid Truyts, Rosa Maria Affonso Moysés, Luciene Machado dos Reis & Vanda Jorgetti

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  1. Flavia Ramos de Siqueira
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Contributions

VJ conceived and design research. WVD and LMR performed experiments. FRS and CAMT analyzed the data. FRS interpreted results of experiments. FRS prepared figures and drafted the manuscript. FRS, KCO, and VJ edited and revised the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Vanda Jorgetti.

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Siqueira, F.R.d., Oliveira, K.C.d., Dominguez, W.V. et al. Effect of parathyroidectomy on bone tissue biomarkers and body composition in patients with chronic kidney disease and secondary hyperparathyroidism. Eur J Clin Nutr 75, 1126–1133 (2021). https://doi.org/10.1038/s41430-020-00829-7

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