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Microcirculatory changes and skeletal muscle oxygenation measured at rest by non-infrared spectroscopy in patients with and without diabetes undergoing haemodialysis

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Abstract

Introduction

Haemodialysis has direct and indirect effects on skin and muscle microcirculatory regulation that are severe enough to worsen tolerance to physical exercise and muscle asthenia in patients undergoing dialysis, thus compromising patients' quality of life and increasing the risk of mortality. In diabetes these circumstances are further complicated, leading to an approximately sixfold increase in the incidence of critical limb ischaemia and amputation. Our aim in this study was to investigate in vivo whether haemodialysis induces major changes in skeletal muscle oxygenation and blood flow, microvascular compliance and tissue metabolic rate in patients with and without diabetes.

Methods

The study included 20 consecutive patients with and without diabetes undergoing haemodialysis at Sant Andrea University Hospital, Rome from March to April 2007. Near-infrared spectroscopy (NIRS) quantitative measurements of tissue haemoglobin concentrations in oxygenated [HbO2] and deoxygenated forms [HHb] were obtained in the calf once hourly for 4 hours during dialysis. Consecutive venous occlusions allowed one to obtain muscular blood flow (mBF), microvascular compliance and muscle oxygen consumption (mVO2). The tissue oxygen saturation (StO2) and content (CtO2) as well as the microvascular bed volume were derived from the haemoglobin concentration. Nonparametric tests were used to compare data within each group and among the groups and with a group of 22 matched healthy controls.

Results

The total haemoglobin concentration and [HHb] increased significantly during dialysis in patients without and with diabetes. Only in patients with diabetes, dialysis involved a [HbO2], CtO2 and increase but left mVO2 unchanged. Multiple regression StO2 analysis disclosed a significant direct correlation of StO2 with HbO2 and an inverse correlation with mVO2. Dialysis increased mBF only in diabetic patients. Microvascular compliance decreased rapidly and significantly during the first hour of dialysis in both groups.

Conclusions

Our NIRS findings suggest that haemodialysis in subjects at rest brings about major changes in skeletal muscle oxygenation, blood flow, microvascular compliance and tissue metabolic rate. These changes differ in patients with and without diabetes. In all patients haemodialysis induces changes in tissue haemoglobin concentrations and microvascular compliance, whereas in patients with diabetes it alters tissue blood flow, tissue oxygenation (CtO2, [HbO2]) and the metabolic rate (mVO2). In these patients the mVO2 is correlated to the blood supply. The effects of haemodialysis on cell damage remain to be clarified. The absence of StO2 changes is probably linked to an opposite [HbO2] and mVO2 pattern.

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Abbreviations

CtO2:

tissue oxygen content

Hb:

haemoglobin

[HbO2]:

oxygenated tissue haemoglobin concentration

[HbT]:

total haemoglobin concentration

[HHb]:

deoxygenated tissue haemoglobin concentration

mBF:

muscular blood flow

mHF:

muscular haemoglobin flow

mVO2:

muscle oxygen consumption

NIRS:

near-infrared spectroscopy

StO2:

tissue oxygen saturation.

References

  1. Kemp GJ, Crowe AV, Anijeet HK, Gong QY, Bimson WE, Frostick SP, Bone JM, Bell GM, Roberts JN: Abnormal mitochondrial function and muscle wasting, but normal contractile efficiency, in haemodialysed patients studied non-invasively in vivo. Nephrol Dial Transplant. 2004, 19: 1520-1527. 10.1093/ndt/gfh189.

    Article  PubMed  Google Scholar 

  2. Kouidi E, Albani M, Natsis K, Megalopoulos A, Gigis P, Guiba-Tziampiri O, Tourkantonis A, Deligiannis A: The effects of exercise training on muscle atrophy in haemodialysis patients. Nephrol Dial Transplant. 1998, 13: 685-699. 10.1093/ndt/13.3.685.

    Article  CAS  PubMed  Google Scholar 

  3. Brodin E, Ljungman S, Hedberg M, Sunnerhagen KS: Physical activity, muscle performance and quality of life in patients treated with chronic peritoneal dialysis. Scand J Urol Nephrol. 2001, 35: 71-78. 10.1080/00365590151030886.

    Article  CAS  PubMed  Google Scholar 

  4. Sietsema KE, Amato A, Adler SG, Brass EP: Exercise capacity as a predictor of survival among ambulatory patients with ESRD. Kidney Int. 2004, 65: 719-724. 10.1111/j.1523-1755.2004.00411.x.

    Article  PubMed  Google Scholar 

  5. Johansen KL: Physical functioning and exercise capacity in patients on dyalisis. Adv Ren Replace Ther. 1999, 6: 141-148.

    CAS  PubMed  Google Scholar 

  6. Pannier B, Guerin AP, Marchais SJ, Metivier F, Safar ME, London GM: Postischemic vasodilation, endothelial activation and cardiovascular remodelling in end-stage renal disease. Kidney Int. 2000, 57: 1091-1099. 10.1046/j.1523-1755.2000.00936.x.

    Article  CAS  PubMed  Google Scholar 

  7. London GM, Pannier B, Agharazii M, Guerin AP, Verbke FH, Marchais SJ: Forearm reactive hyperemia and mortalità in end-stage renal disease. Kidney Int. 2004, 65: 700-704. 10.1111/j.1523-1755.2004.00434.x.

    Article  PubMed  Google Scholar 

  8. Passauer J, Pistrosch F, Büssemaker E, Lässig G, Herbrig K, Gross P: Reduced agonist-induced endothelium-dependent vasodilation in uremia is attributable to an impairment of vascular nitric oxide. J Am Soc Nephrol. 2005, 16: 959-965. 10.1681/ASN.2004070582.

    Article  CAS  PubMed  Google Scholar 

  9. Marrades RM, Roca J, Campistol JM, Diaz O, Barberá JA, Torregrosa JV, Masclans JR, Cobos A, Rodríguez-Roisin R, Wagner PD: Effects of erythropoietin on muscle O2 transport during exercise in patients with chronic renal failure. J Clin Invest. 1996, 97: 2092-2100. 10.1172/JCI118646.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. De Blasi RA, Palmisani S, Alampi D, Mercieri M, Romano R, Collini S, Pinto G: Microvascular dysfunction and skeletal muscle oxygenation assessed by phase-modulation near-infrared spectroscopy in patients with septic shock. Intensive Care Med. 2005, 31: 1661-1668. 10.1007/s00134-005-2822-y.

    Article  PubMed  Google Scholar 

  11. Schalkwijk CG, Stehouwer CD: Vascular complications in diabetes mellitus: the role of endothelial dysfunction. Clin Sci (Lond). 2005, 109: 143-159. 10.1042/CS20050025.

    Article  CAS  Google Scholar 

  12. Morbach S, Quante C, Ochs HR, Gaschler F, Pallast J-M, Knevels U: Increased risk of lower-extremity amputation among Caucasian diabetic patients on dialysis. Diabetes Care. 2001, 24: 1689-1670. 10.2337/diacare.24.9.1689.

    Article  CAS  PubMed  Google Scholar 

  13. McGrath NM, Curran BA: Recent commencement of dialysis is a risk factor for lower-extremity amputation in a high-risk diabetic population. Diabetes Care. 2000, 23: 432-433. 10.2337/diacare.23.3.432.

    Article  CAS  PubMed  Google Scholar 

  14. Bos WJW, Buin Sjoerd, van Older RW, Keur I, Wesseling KH, Westerhof N, Krediet RT, Aritsz LA: Cardiac and hemodynamic effects of hemodialysis and ultrafiltration. Am J Kidney Dis. 2000, 35: 819-826. 10.1016/S0272-6386(00)70250-2.

    Article  CAS  PubMed  Google Scholar 

  15. Converse RL, Jacobsen TN, Fouad-Tarazi F, Obregon TM, Toto RD, Victor RG: Paradoxical withdrawal of reflex vasoconstriction as a cause of hemodialysis-induced hypotension. J Clin Invest. 1992, 90: 1657-1665. 10.1172/JCI116037.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Sande van der FM, Kooman JP, van Kuijk WHM, Leunissen KML: Management of hypotension in dialysis patients: role of dialysate temperature control. Saudi J Kidney Dis Transplant. 2001, 12: 328-386.

    Google Scholar 

  17. Rovati L, Bandera A, Donini M, Salvatori G: Design and performance of a wide-bandwidth and sensitive instrument for near-infrared spectroscopic measurements on human tissue. Rev Sci Instrum. 2004, 75: 5315-5325. 10.1063/1.1818588.

    Article  CAS  Google Scholar 

  18. Matcher S, Cope M, Delpy D: Use of the water absorption spectrum to quantify tissue chromophore concentration changes in near infrared spectroscopy. Phys Med Biol. 1993, 38: 177-196.

    Google Scholar 

  19. Van Beekvelt M, Borghuis M, Van Engelen B, Wevers R, Collier W: Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci (Lond). 2001, 101: 21-28. 10.1042/CS20000247.

    Article  CAS  Google Scholar 

  20. Martelli F, Del Bianco S, Zaccanti G: Effect of the refractive index mismatch on light propagation through diffusive layered media. Phys Rev E Stat Nonlin Soft Matter Phys. 2004, 70: 011907-

    Article  PubMed  Google Scholar 

  21. Simpson CR, Kohl M, Essenpreis M, Cope M: Near-infrared optical properties of ex vivo human skin and subcutaneous tissues measured using the Monte Carlo inversion technique. Phys Med Biol. 1998, 43: 2465-2478. 10.1088/0031-9155/43/9/003.

    Article  CAS  PubMed  Google Scholar 

  22. Castaneda-Sceppa C, Sarnak MJ, Wang X, Greene T, Madero M, Kusek JW, Beck G, Kopple JD, Levey AS, Menon V: Role of adipose tissue in determining muscle mass in patients with chronic kidney disease. J Renal Nutr. 2007, 17: 314-322. 10.1053/j.jrn.2007.05.006.

    Article  Google Scholar 

  23. Klitzman B, Duling BR: Microvascular hematocrit and red cell flow in resting and contracting striated muscle. Am J Physiol. 1979, 237: H481-H490.

    CAS  PubMed  Google Scholar 

  24. De Blasi RA, Ferrari M, Natali A, Conti G, Mega A, Gasparetto A: Noninvasive measurement of forearm blood flow and oxygen consumption by near-infrared spectroscopy. J Appl Physiol. 1994, 76: 1388-1393.

    CAS  PubMed  Google Scholar 

  25. Wolf U, Wolf M, Choi JH, Levi M, Choudhury D, Hull S, Coussirat D, Paunescu LA, Safonova LP, Michalos A, Mantulin WW, Gratton E: Localized irregularities in haemoglobin flow and oxygenation in calf muscle in patients with peripheral vascular disease detected with near-infrared spectrophotometry. J Vasc Surg. 2003, 37: 1017-1026. 10.1067/mva.2003.214.

    Article  PubMed  Google Scholar 

  26. Weiss T, Windthorst C, Weiss C, Kreuzer J, Bomber J, Kübler W: Acute effects of haemodialysis on cutaneous microcirculation in patients with peripheral arterial occlusive disease. Nephrol Dial Transplant. 1998, 13: 2317-2321. 10.1093/ndt/13.9.2317.

    Article  CAS  PubMed  Google Scholar 

  27. Hinchliffe RJ, Kirk B, Bhattacharjee D, Roe S, Jeffcoate W, Game F: The effect of haemodialysis on transcutaneous oxygen tension in patients with diabetes - a pilot study. Nephrol Dial Transplant. 2006, 21: 1981-1983. 10.1093/ndt/gfl241.

    Article  PubMed  Google Scholar 

  28. Abu-Hamdan DK, Desai SG, Mahajan SK, Muller BF, Briggs WA, Lynne-Davies P, McDonald FD: Hypoxemia during haemodialysis using acetate versus bicarbonate dialysate. Am J Nephrol. 1984, 4: 248-253. 10.1159/000166818.

    Article  CAS  PubMed  Google Scholar 

  29. Pitcher WD, Diamond SM, Henrich WL: Pulmonary gas exchange during dialysis in patients with obstructive lung disease. Chest. 1989, 96: 1136-1141. 10.1378/chest.96.5.1136.

    Article  CAS  PubMed  Google Scholar 

  30. Hamaoka T, McCully KK, Quaresima V, Yamamoto K, Chance B: Near-infrared spectroscopy/imaging for monitoring muscle oxygenation and oxidative metabolism in healthy and diseased humans. J Biomed Opt. 2007, 12: 62105-10.1117/1.2805437.

    Article  Google Scholar 

  31. Rooke TW, Osmundson PJ: The influence of age, sex, smoking, and diabetes on lower limb transcutaneous oxygen tension in patients with arterial occlusive disease. Arch Intern Med. 1990, 150: 129-132. 10.1001/archinte.150.1.129.

    Article  CAS  PubMed  Google Scholar 

  32. Sala E, Noyszewski EA, Campistol JM, Marrades RM, Dreha S, Torregrossa JV, Beers JS, Wagner PD, Roca J: Impaired muscle oxygen transfer in patients with chronic renal failure. Am J Physiol Regul Integr Comp Physiol. 2001, 280: R1240-R1248.

    CAS  PubMed  Google Scholar 

  33. Schneditz D, Zaluska WT, Morris AT, Levin NW: Effects of ultra-filtration on peripheral urea sequestration in haemodialysis patients. Nephrol Dial Transplant. 2001, 16: 994-998. 10.1093/ndt/16.5.994.

    Article  CAS  PubMed  Google Scholar 

  34. Hansen J, Victor RG: Direct measurement of sympathetic activity: new insights into disordered blood pressure regulation an chronic renal failure. Curr Opin Nephrol Hypertens. 1994, 3: 636-643. 10.1097/00041552-199411000-00014.

    Article  CAS  PubMed  Google Scholar 

  35. Mancini DM, Bolinger L, Li H Kendrick, Chance B, Wilson JR: Validation of near infrared spectroscopy in humans. J Appl Physiol. 1994, 77: 2740-2747.

    CAS  PubMed  Google Scholar 

  36. Movilli E, Cancarini GC, Cassamali S, Camerini C, Brunori G, Maffei C, Maiorca R: Inter dialytic variations in blood volume and total body water in uraemic patients treated by dialysis. Nephrol Dial Transplant. 2004, 19: 185-189. 10.1093/ndt/gfg494.

    Article  PubMed  Google Scholar 

  37. Jofré R, Rodriguez-Benitez P, López-Gómez JM, Pérez-Garcia R: Inflammatory syndrome in patients on haemodialysis. J Am Soc Nephrol. 2006, 17: 274-280. 10.1681/ASN.2006080926.

    Article  Google Scholar 

  38. Kamimura MA, Draibe SA, Avesani CM, Canziani MEF, Colugnani FAB, Cuppari L: Resting energy expenditure and its determinants in haemodialysis patients. Eur J Clin Nutr. 2007, 61: 362-367. 10.1038/sj.ejcn.1602516.

    Article  CAS  PubMed  Google Scholar 

  39. Minutolo R, De Nicola L, Bellizzi V, Iodice C, Rubino R, Aucella F, Stallone C, Nappi F, Avella F, Maione E, Conte G, Di Iorio BR: Intra- and post-dialytic changes of haemoglobin concentrations in non-anaemic haemodialysis patients. Nephrol Dial Transplant. 2003, 18: 2606-2612. 10.1093/ndt/gfg387.

    Article  CAS  PubMed  Google Scholar 

  40. De Blasi RA, Palmisani S, Boezi M, Arcioni R, Collini S, Troisi F, Pinto G: Effects of remifentanil-based general anaesthesia with propofol or sevoflurane on muscle microcirculation as assessed by near-infrared spectroscopy. Br J Anesth. 2008, 101: 171-177. 10.1093/bja/aen136.

    Article  CAS  Google Scholar 

  41. Perseghin G, Scifo P, De Cobelli F, Pagliato E, Battezzati A, Arcelloni C, Vanzulli A, Testolin G, Pozza G, Del Maschio A, Luzi L: Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes. 1999, 48: 1600-1606. 10.2337/diabetes.48.8.1600.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This article is part of Critical Care Volume 13 Supplement 5: Tissue oxygenation (StO2) in healthy volunteers and critically-ill patients. The full contents of the supplement are available online at http://ccforum.com/supplements/13/S5. Publication of the supplement has been supported with funding from Hutchinson Technology Inc.

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Authors and Affiliations

  1. Department of Anaesthesiology and Intensive Care, II Faculty of Medicine University 'La Sapienza', Via di Grottarossa 1035, 00189, Rome, Italy

    Roberto Alberto De Blasi, Roberto Arcioni & Marta Boezi

  2. Department of Nephro-Urology, II Faculty of Medicine University 'La Sapienza', Via di Grottarossa 1035, 00189, Rome, Italy

    Remo Luciani, Giorgio Punzo & Paolo Menè

  3. Department of Neuroscience, Marche University Politecnica, Via Tronto 10/A, 60100, Ancona, Italy

    Rocco Romano

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  1. Roberto Alberto De Blasi
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  2. Remo Luciani
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Correspondence to Roberto Alberto De Blasi.

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De Blasi, R.A., Luciani, R., Punzo, G. et al. Microcirculatory changes and skeletal muscle oxygenation measured at rest by non-infrared spectroscopy in patients with and without diabetes undergoing haemodialysis. Crit Care 13 (Suppl 5), S9 (2009). https://doi.org/10.1186/cc8007

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