Effects of dietary intake and nutritional status on cerebral oxygenation in patients with chronic kidney disease not undergoing dialysis: A cross-sectional study

Autoři: Susumu Ookawara aff001;  Yoshio Kaku aff001;  Kiyonori Ito aff001;  Kanako Kizukuri aff002;  Aiko Namikawa aff002;  Shinobu Nakahara aff002;  Yuko Horiuchi aff002;  Nagisa Inose aff002;  Mayako Miyahara aff002;  Michiko Shiina aff002;  Saori Minato aff001;  Mitsutoshi Shindo aff001;  Haruhisa Miyazawa aff001;  Keiji Hirai aff001;  Taro Hoshino aff001;  Miho Murakoshi aff002;  Kaoru Tabei aff003;  Yoshiyuki Morishita aff001
Působiště autorů: Division of Nephrology, First Department of Integrated Medicine, Saitama Medical Center, Jichi Medical University, Saitama, Japan aff001;  Department of Nutrition, Saitama Medical Center, Jichi Medical University, Saitama, Japan aff002;  Department of Internal Medicine, Minami-uonuma City Hospital, Niigata, Japan aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223605



Dietary management is highly important for the maintenance of renal function in patients with chronic kidney disease (CKD). Cerebral oxygen saturation (rSO2) was reportedly associated with the estimated glomerular filtration rate (eGFR) and cognitive function. However, data concerning the association between cerebral rSO2 and dietary intake of CKD patients is limited.


This was a single-center observational study. We recruited 67 CKD patients not undergoing dialysis. Cerebral rSO2 was monitored using the INVOS 5100c oxygen saturation monitor. Energy intake was evaluated by dietitians based on 3-day meal records. Daily protein and salt intakes were calculated from 24-h urine collection.


Multivariable regression analysis showed that cerebral rSO2 was independently associated with energy intake (standardized coefficient: 0.370) and serum albumin concentration (standardized coefficient: 0.236) in Model 1 using parameters with p < 0.10 in simple linear regression analysis (body mass index, Hb level, serum albumin concentration, salt and energy intake) and confounding factors (eGFR, serum sodium concentration, protein intake), and the energy/salt index (standardized coefficient: 0.343) and Hb level (standardized coefficient: 0.284) in Model 2 using energy/protein index as indicated by energy intake/protein intake and energy/salt index by energy intake/salt intake in place of salt, protein and energy intake.


Cerebral rSO2 is affected by energy intake, energy/salt index, serum albumin concentration and Hb level. Sufficient energy intake and adequate salt restriction is important to prevent deterioration of cerebral oxygenation, which might contribute to the maintenance of cognitive function in addition to the prevention of renal dysfunction in CKD patients.

Klíčová slova:

Chronic kidney disease – Oxygen – Renal system – Serum albumin – Serum proteins – Urine – Sodium chloride


1. Japanese Society of Nephrology, eds. Clinical Practice Guidebook for Diagnosis and Treatment of Chronic Kidney Disease 2012. Tokyo, Japan: Tokyo-Igakusya; 2012.

2. Kopple JD. National kidney foundation K/DOQI clinical practice guidelines for nutrition in chronic renal failure. Am J Kidney Dis. 2001; 37(1 Suppl 2): S66–70.

3. Academy of Nutrition and Dietetics. Evidence-based nutrition practice guidelines. Chronic kidney disease (CKD). 2010. (https://www.andeal.org/template.cfm?template=guide_summary&key=2410&highlight=CKD%20energy&home=1#supportevidence).

4. Fouque D, Laville M, Boissel JP. Low protein diets for chronic kidney disease in non diabetic adults. Cochrane Database Syst Rev. 2009; CD001892. doi: 10.1002/14651858.CD001892.pub3 19588328

5. Robertson L, Waugh N, Robertson A. Protein restriction for diabetic renal disease. Cochrane Database Syst Rev. 2007; CD002181. doi: 10.1002/14651858.CD002181.pub2 17943769

6. Kidney disease: Improving global outcomes (KDOQI) CKD work group. KDIGO 2012 Clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney Int Suppl. 2013; 3: 1–150.

7. Swift PA, Markandu ND, Sagnella GA, He FJ, MacGregor GA. Modest salt reduction reduces blood pressure and urine protein excretion in black hypertensives: a randomized control trial. Hypertension. 2005; 46: 308–312. doi: 10.1161/01.HYP.0000172662.12480.7f 15983240

8. Slagman MCJ, Waanders F, Hemmelder MH, Woittiez AJ, Janssen WM, Lambers Heerspink HJ, et al. Moderate dietary sodium restriction added to angiotensin converting enzyme inhibition compared with dual blockade in lowering proteinuria and blood pressure: randomized controlled trial. BMJ. 2011; 343: d4366. doi: 10.1136/bmj.d4366 21791491

9. Duenhas MR, Draibe SA, Avesani CM, Sesso R, Cuppari L. Influence of renal function on spontaneous dietary intake and on nutritional status of chronic renal insufficiency patients. Eur J Clin Nutr. 2003; 57: 1473–1478. doi: 10.1038/sj.ejcn.1601713 14576761

10. Huang MC, Chen ME, Hung HC, Chen HC, Chang WT, Lee CH, et al. Inadequate energy and excess protein intakes may be associated with worsening renal function in chronic kidney disease. J Ren Nutr. 2008; 18: 187–194. doi: 10.1053/j.jrn.2007.08.003 18267211

11. Lin J, Hu FB, Curhan GC. Association of diet with albuminuria and kidney function decline. Clin J Am Soc Nephrol. 2010; 5: 836–843. doi: 10.2215/CJN.08001109 20299364

12. Vegter S, Perna A, Postma MJ, Navis G, Remuzzi G, Ruggenenti P. Sodium intake, ACE inhibition, and progression to ESRD. J Am Soc Nephrol. 2012; 23: 165–173. doi: 10.1681/ASN.2011040430 22135311

13. Prohovnik I, Post J, Uribarri J, Lee H, Sandu O, Langhoff E. Cerebrovascular effects of hemodialysis in chronic kidney disease. J Cereb Blood Flow Metab. 2007; 27: 1861–1869. doi: 10.1038/sj.jcbfm.9600478 17406658

14. Hoshino T, Ookawara S, Goto S, Miyazawa H, Ito K, Ueda Y, et al. Evaluation of cerebral oxygenation in patients undergoing long-term hemodialysis. Nephron Clin Pract. 2014; 126: 57–61. doi: 10.1159/000358432 24526002

15. Ito K, Ookawara S, Ueda Y, Goto S, Miyazawa H, Yamada H, et al. Factors affecting cerebral oxygenation in hemodialysis patients: cerebral oxygenation associates with pH, hemodialysis duration, serum albumin concentration, and diabetes mellitus. PLoS One. 2015; 10: e0117474. doi: 10.1371/journal.pone.0117474 25706868

16. Kovarova L, Valerianova A, Kmentova T, Lachmanova J, Hladinova Z, Malik J. Low cerebral oxygenation Is associated with cognitive impairment in chronic hemodialysis patients. Nephron. 2018; 139: 113–119. doi: 10.1159/000487092 29439251

17. Miyazawa H, Ookawara S, Ito K, Ueda Y, Yanai K, Ishii H, et al. Association of cerebral oxygenation with estimated glomerular filtration rate and cognitive function in chronic kidney disease patients without dialysis therapy. PLoS One. 2018; 13: e0199366. doi: 10.1371/journal.pone.0199366 29940017

18. Matsuo S, Imai E, Horio M, Yasuda Y, Tomino K, Nitta K, et al. Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis. 2009; 53: 982–992. doi: 10.1053/j.ajkd.2008.12.034 19339088

19. Resource Council, eds. Standard Tables of Food Composition in Japan, 5st ed. Tokyo, Japan: Resource Council, Science and Technology Agency; 2012. (in Japanese).

20. Maroni BJ, Steinman TI, Mitch WE. A method for estimating nitrogen intake of patients with chronic renal failure. Kidney Int. 1985; 27: 58–65 doi: 10.1038/ki.1985.10 3981873

21. Tobias JD. Cerebral oxygenation monitoring: near-infrared spectroscopy. Expert Rev Med Devices. 2006; 3: 235–243. doi: 10.1586/17434440.3.2.235 16515389

22. Ferrari M, Mottola L, Quaresima V. Principles, techniques, and limitations of near infrared spectroscopy. Can J Appl Physiol. 2004; 29: 463–487. 15328595

23. Lemmers PMA, Toet MC, van Bel F. Impact of patent ductus arteriosus and subsequent therapy with indomethacin on cerebral oxygenation in preterm infants. Pediatrics. 2008; 121: 142–147. doi: 10.1542/peds.2007-0925 18166568

24. Hyttel-Sorensen S, Sorensen LC, Riera J, Greisen G. Tissue oximetry: a comparison of mean values of regional tissue saturation, reproducibility and dynamic range of four NIRS-instruments on the human forearm. Biomed Opt Express. 2011; 2: 3047–3057. doi: 10.1364/BOE.2.003047 22076266

25. Schmitz J, Pichler G, Schwaberger B, Urlesberger B, Baik N, Binder C. Feasibility of long-term cerebral and peripheral regional tissue oxygen saturation measurements. Physiol Meas. 2014; 35: 1349–1355. doi: 10.1088/0967-3334/35/7/1349 24854420

26. Hongo K, Kobayashi S, Okudera H, Hokama M, Nakagawa F. Noninvasive cerebral optical spectroscopy: depth-resolved measurements of cerebral haemodynamics using indocyanine green. Neuro Res. 1995; 17: 89–93.

27. Maslehaty H, Krause-Tilz U, Petridis AK, Barth H, Mehdorn HM. Continuous measurement of cerebral oxygenation with near-infrared spectroscopy after spontaneous subarachnoid hemorrhage. ISRN Neurol. 2012; 907187. doi: 10.5402/2012/907187 23209938

28. Gomez-Pinilla F. Brain foods: the effect of nutrients on brain function. Nat Rev Neurosci. 2008; 9: 568–578. doi: 10.1038/nrn2421 18568016

29. Konturek SJ, Konturek JW, Pawlik T, Brzozowki T. Brain-gut axis and its role in the control of food intake. J Physiol Pharmacol. 2004; 55: 137–154. 15082874

30. Meier U, Gressner AM. Endocrine regulation of energy metabolism: review of pathobiochemical and clinical chemical aspects of leptin, ghrelin, adiponectin, and resistin. Clin Chem. 2004; 50: 1511–1525. doi: 10.1373/clinchem.2004.032482 15265818

31. Gualillo O, Laga F, Gomez-Reino J, Casanueva FF, Diguez C. Ghrelin, a widespread hormone: insights into molecular and cellular regulation of its expression and metabolism of action. FEBS Lett. 2003; 552: 105–109. doi: 10.1016/s0014-5793(03)00965-7 14527669

32. Teauro M, Schinzar F, Caramanti M, Lauro R, Cardillo C. Cardiovascular and metabolic effects of ghrelin. Curr. Diabetes Rev. 2010; 6: 228–235. 20459393

33. Virdis A, Lerman LO, Regoli F, Ghiadoni L, Lerman A. Human ghrelin: A gastric hormone with cardiovascular properties. Curr Pharm Des. 2016; 22: 52–58. doi: 10.2174/1381612822666151119144458 26581223

34. Wang Y, Narsinh K, Zhao L, Sun D, Wang D, Zhang Z, et al. Effects and mechanisms of ghrelin on cardiac microvascular endothelial cells in rats. Cell Biol Int. 2011; 35: 135–140. doi: 10.1042/CBI20100139 20843299

35. Zhao H, Liu G, Wang Q, Ding L, Cai H, Jiang H, et al. Effect of ghrelin on human endothelial cells apoptosis induced by high glucose. Biochem Biophys Res Commun. 2007; 362: 677–681. doi: 10.1016/j.bbrc.2007.08.021 17719561

36. Cheung WW, Mak RH. Ghrelin in chronic kidney disease. Int J Pept. 2010; pii: 567343.

37. Gupta RK, Kuppusamy TK, Patrie JT, Gaylinn B, Thomer MO, Bolton WK. Association of plasma des-acyl ghrelin levels with CKD. Clin J Am Nephrol. 2013; 8: 1098–1105.

38. Wynne K, Giannitsopoulou K, Small CJ, Patterson M, Frost G, Ghatei MA, et al. Subcutaneous ghrelin enhances acute food intake in malnourished patients who receive maintenance peritoneal dialysis: A randomized, placebo-controlled trial. J Am Soc Nephrol. 2005; 16: 2111–2118. doi: 10.1681/ASN.2005010039 15888560

39. Ashby DR, Ford HE, Wynne KJ, Wren AM, Murphy KG, Busbridge M, et al. Sustained appetite improvement in malnourished dialysis patients by daily ghrelin treatment. Kidney Int. 2009; 76: 199–206. doi: 10.1038/ki.2009.114 19387475

40. Heye AK, Thrippleton MJ, Chappell FM, Hemandez Mdel C, Armitage PA, Makin SD, et al. Blood pressure and sodium: association with MRI markers in cerebral small vessel disease. J Cereb Blood Flow Metab. 2016; 36: 264–274. doi: 10.1038/jcbfm.2015.64 25899292

41. Strazzullo P, D’Elia L, Kandala NB, Cappucio EP. Salt intake, stroke, and cardiovascular disease: meta-analysis of prospective studies. BMJ. 2009; 339: b4567. doi: 10.1136/bmj.b4567 19934192

42. Faraco G, Brea D, Garcia-Bonilla L, Wang G, Racchumi G, Chang H, et al. Dietary salt promotes neurovascular and cognitive dysfunction through a gut-initiated TH17 response. Nat Neurosci. 2018; 21: 240–249. doi: 10.1038/s41593-017-0059-z 29335605

43. Ookawara S, Sato H, Takeda H, Tabei K. Methods for approximating colloid osmotic pressure in long-term hemodialysis patients. Ther Apher Dial. 2014; 18: 202–207. doi: 10.1111/1744-9987.12070 24720412

44. Yuruk K, Bartels SA, Milstein DM, Bezemer R, Biemond BJ, Ince C. Red blood cell transfusions and tissue oxygenation in anemic hematology outpatients. Transfusion. 2012; 52: 641–646. doi: 10.1111/j.1537-2995.2011.03312.x 21883269

45. Torella F, Haynes SL, McCollum CN. Cerebral and peripheral oxygen saturation during red cell transfusion. J Surg Res. 2003; 110: 217–221. doi: 10.1016/s0022-4804(03)00037-4 12697404

46. van Hoften JC, Verhagen EA, Keating P, ter Horst HJ, Bos AF. Cerebral tissue oxygen saturation and extraction in preterm infants before and after blood transfusion. Arch Dis Child Fetal Neonatal Ed. 2010; 95: F352–F358. doi: 10.1136/adc.2009.163592 20466739

47. Dhabangi A, Ainomugisha B, Cserti-Gazdewich C, Ddungu H, Kyeyune D, Musisi E, et al. Cerebral oximetry in Ugandan children with severe anemia: Clinical categories and response to transfusion. JAMA Pediatr. 2016; 170: 995–1002. doi: 10.1001/jamapediatrics.2016.1254 27532507

48. Neunhoeffer F, Hofbeck M, Schuhmann MU, Fuchs J, Schlensak C, Esslinger M, et al. Cerebral oxygen metabolism before and after RBC transfusion in infants following major surgical procedures. Pediatr Crit Care Med. 2018; 19: 318–327. doi: 10.1097/PCC.0000000000001483 29406374

49. Ito K, Ookawara S, Ueda Y, Miyazawa H, Kofuji M, Hayasaka H, et al. Changes in cerebral oxygenation associated with intradialytic blood transfusion in patients with severe anemia undergoing hemodialysis. Nephron Extra. 2017; 7: 42–51. doi: 10.1159/000471812 28559914

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden