Transperitoneal administration of hydrogen suppresses peritoneal and systemic oxidative stressScientific Research

Transperitoneal administration of dissolved hydrogen for peritoneal dialysis patients: a novel approach to suppress oxidative stress in the peritoneal cavity

https://medicalgasresearch.biomedcentral.com/articles/10.1186/2045-9912-3-14

Abstract

Background

Oxidative stress (OS) associated with glucose breakdown products such as methylglyoxal has been reported to be associated with worsening peritoneal function in patients treated with peritoneal dialysis (PD). However, the use of antioxidants in general is limited due to their deleterious effects. This study aimed to elucidate the effects of a novel antioxidant molecular hydrogen (H2) on peritoneal OS using albumin redox status as a marker.

Methods

Effluent and blood samples from 6 normal PD patients were obtained during peritoneal equilibration testing using standard dialysate and hydrogen-rich dialysate. Determination of the redox state of albumin in wastewater and blood using high performance liquid chromatography.

Results

The H2-enriched dialysate (62.31 ± 11.10%) had significantly higher mean fractions of reduced albumin (ƒ(HMA)) in the effluent than the standard dialysate (54.70 ± 13.08%). Likewise, serum ƒ(HMA) was significantly higher in hydrogen-rich dialysate (65.75 ± 7.52%) than in standard dialysate (62.44 ± 7.66%).

Conclusion

Intraperitoneal administration of H2 reduces peritoneal and systemic OS.

References

  1. Yamamoto R, Otsuka Y, Nakayama M, Maruyama Y, Katoh N, Ikeda M, Yamamoto H, Yokoyama K, Kawaguchi Y, Matsushima M: Risk factors for encapsulating peritoneal sclerosis in patients who have experienced peritoneal dialysis treatment. Clin Exp Nephrol. 2005, 9: 148-152. 10.1007/s10157-005-0349-8.

    PubMed Article Google Scholar

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    PubMed Google Scholar

  3. Glomb MA, Monnier VM: Mechanism of protein modification by glyoxal and glycoaldehyde, reactive intermediates of the Maillard reaction. J Biol Cham. 1995, 270: 10017-10026. 10.1074/jbc.270.17.10017.

    CAS Article Google Scholar

  4. Nakayama M, Saito K, Sato E, Nakayama K, Terawaki H, Ito S, Kohno M: Radical generation by the non-enzymatic reaction of methylglyoxal and hydrogen peroxide. Redox Rep. 2007, 12: 125-133. 10.1179/135100007X200182.

    CAS PubMed Article Google Scholar

  5. Terawaki H, Nakao M, Nakayama K, Nakayama M, Kimura A, Takane K, Mitome J, Hamaguchi A, Ogura M, Yokoyama K, Ito S, Hosoya T: Peritoneal clearance and transport of methylglyoxal. Nephrol Dial Transplant. 2011, 26: 753-754. 10.1093/ndt/gfq698.

    PubMed Article Google Scholar

  6. Kawanishi H, Nakayama M, Miyazaki M, Honda K, Tomo T, Kasai K, Nakamoto H: NEXT-PD Study Group: Prospective multicenter observational study of encapsulating peritoneal sclerosis with neutral dialysis solution – the NEXT-PD study. Adv Perit Dial. 2010, 26: 71-74.

    PubMed Google Scholar

  7. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S: Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med. 2007, 13: 688-694. 10.1038/nm1577.

    CAS PubMed Article Google Scholar

  8. Abraini JH, Gardette-Chauffour MC, Martinez E, Rostain JC, Lemaire C: Psychophysiological reactions in humans during an open sea dive to 500 m with a hydrogen-helium-oxygen mixture. J Appl Physiol. 1994, 76: 1113-1118.

    CAS PubMed Google Scholar

  9. Fontanari P, Badier M, Guillot C, Tomei C, Burnet H, Gardette B, Jammes Y: Changes in maximal performance of inspiratory and skeletal muscles during and after the 7.1-MPa Hydra 10 record human dive. Eur J Appl Physiol. 2000, 81: 325-328. 10.1007/s004210050050.

    CAS PubMed Article Google Scholar

  10. Ohta S: Recent progress toward hydrogen medicine: potential of molecular hydrogen for preventive and therapeutic applications. Curr Pharm Des. 2011, 17: 2241-52. 10.2174/138161211797052664.

    CAS PubMed Central PubMed Article Google Scholar

  11. Abe T, Li XK, Yazawa K, Hatayama N, Xie L, Sato B, Kakuta Y, Tsutahara K, Okumi M, Tsuda H, Kaimori JY, Isaka Y, Natori M, Takahara S, Nonomura N: Hydrogen-rich University of Wisconsin solution attenuates renal cold ischemia-reperfusion injury. Transplantation. 2012, 94: 14-21.

    CAS PubMed Article Google Scholar

  12. American Heart Association: Criteria for the evaluation of the severity of established renal disease: Report of the council on the kidney in cardiovascular diseases. Circulation. 1971, 44: 306-307.

    Article Google Scholar

  13. Twardowski ZJ: PET-a simpler approach for determining prescriptions for adequate dialysis therapy. Adv Perit Dial. 1990, 6: 186-191.

    CAS PubMed Google Scholar

  14. Terawaki H, Takada Y, Era S, Funakoshi Y, Nakayama K, Nakayama M, Ogura M, Ito S, Hosoya T: The redox state of albumin and serious cardiovascular incidence in hemodialysis patients. Ther Apher Dial. 2010, 14: 465-471. 10.1111/j.1744-9987.2010.00841.x.

    PubMed Article Google Scholar

  15. Ishibashi Y, Sugimoto T, Ichikawa Y, Akatsuka A, Miyata T, Nangaku M, Tagawa H, Kurokawa K: Glucose dialysate induces mitochondrial DNA damage in peritoneal mesothelial cells. Perit Dial Int. 2002, 22: 11-21.

    PubMed Google Scholar

  16. Lee HB, Yu MR, Song JS, Ha H: Reactive oxygen species amplify protein kinase C signaling in high glucose-induced fibronectin expression by human peritoneal mesothelial cells. Kidney Int. 2004, 65: 1170-1179. 10.1111/j.1523-1755.2004.00491.x.

    CAS PubMed Article Google Scholar

  17. Gunal AI, Celiker H, Ustundag B, Akpolat N, Dogukan A, Akcicek F: The effect of oxidative stress inhibition with trimetazidine on the peritoneal alterations induced by hypertonic peritoneal dialysis solution. J Nephrol. 2003, 16: 225-230.

    CAS PubMed Google Scholar

  18. Shi P, Sun W, Shi P: A hypothesis on chemical mechanism of the effect of hydrogen. Med Gas Res. 2012, 2: 17-10.1186/2045-9912-2-17.

    CAS PubMed Central PubMed Article Google Scholar

  19. Ohsawa I, Nishimaki K, Yamagata K, Ishikawa M, Ohta S: Consumption of hydrogen water prevents atherosclerosis in apolipoprotein E knockout mice. Biochem Biophys Res Commun. 2008, 377: 1195-1198. 10.1016/j.bbrc.2008.10.156.

    CAS PubMed Article Google Scholar

  20. Sato Y, Kajiyama S, Amano A, Kondo Y, Sasaki T, Handa S, Takahashi R, Fukui M, Hasegawa G, Nakamura N, Fujinawa H, Mori T, Ohta M, Obayashi H, Maruyama N, Ishigami A: Hydrogen-rich pure water prevents superoxide formation in brain slices of vitamin C-depleted SMP30/GNL knockout mice. Biochem Biophys Res Commun. 2008, 375: 346-350. 10.1016/j.bbrc.2008.08.020.

    CAS PubMed Article Google Scholar

  21. Nakashima-Kamimura N, Mori T, Ohsawa I, Asoh S, Ohta S: Molecular hydrogen alleviates nephrotoxicity induced by anti-cancer drug cisplatin without compromising anti-tumor activity in mice. Cancer Chemother Pharmacol. 2009, 64: 753-761. 10.1007/s00280-008-0924-2.

    CAS PubMed Article Google Scholar

  22. Cardinal JS, Zhan J, Wang Y, Sugimoto R, Tsung A, McCurry KR, Billar TR, Nakao A: Oral hydrogen water prevents chronic allograft nephropathy in rats. Kidney Int. 2010, 77: 101-109. 10.1038/ki.2009.421.

    CAS PubMed Article Google Scholar

  23. Zhu WJ, Nakayama M, Mori T, Nakayama K, Katoh J, Murata Y, Sato T, Kabayama S, Ito S: Intake of water with high levels of dissolved hydrogen (H2) suppresses ischemia-induced cardio-renal injury in Dahl salt-sensitive rats. Nephrol Dial Transplant. 2011, 26: 2112-2118. 10.1093/ndt/gfq727.

    CAS PubMed Article Google Scholar

  24. Kajiyama S, Hasegawa G, Asano M, Hosoda H, Fukui M, Nakamura N, Kitawaki J, Imai S, Nakano K, Ohta M, Adachi T, Obayashi H, Yoshikawa T: Supplementation of hydrogen-rich water improves lipid and glucose metabolism in patients with type 2 diabetes or impaired glucose tolerance. Nutr Res. 2008, 28: 137-143. 10.1016/j.nutres.2008.01.008.

    CAS PubMed Article Google Scholar

  25. Nakao A, Toyoda Y, Sharma P, Evans M, Guthrie N: Effectiveness of hydrogen rich water on antioxidant status of subjects with potential metabolic syndrome – an open label pilot study. J Clin Biochem Nutr. 2010, 46: 140-149. 10.3164/jcbn.09-100.

    PubMed Central PubMed Article Google Scholar

  26. Ito M, Ibi T, Sahashi K, Ichihara M, Ito M, Ohno K: Open-label trial and randomized, double-blind, placebo-controlled crossover trial of hydrogen-enriched water for mitochondrial and inflammatory myopathies. Med Gas Res. 2011, 1: 24-10.1186/2045-9912-1-24.

    CAS PubMed Central PubMed Article Google Scholar

  27. Ishibashi T, Sato B, Rikitake M, Seo T, Kurokawa R, Hara Y, Naritomi Y, Hara H, Nagao T: Consumption of water containing a high concentration of molecular hydrogen reduces oxidative stress and disease activity in patients with rheumatoid arthritis: an open-label pilot study. Med Gas Res. 2012, 2: 27-10.1186/2045-9912-2-27.

    CAS PubMed Central PubMed Article Google Scholar

  28. Nakayama M, Kabayama S, Nakano H, Zhu WJ, Terawaki H, Nakayama K, Katoh K, Satoh T, Ito S: Biological effect of electrolyzed water in hemodialysis. Nephron Clin Pract. 2009, 112: c9-15. 10.1159/000210569.

    CAS PubMed Article Google Scholar

  29. Nakayama M, Nakano H, Hamada H, Itami N, Nakazawa R, Ito S: A novel bioactive haemodialysis system using dissolved dihydrogen (H2) produced by water electrolysis: a clinical trial. Nephrol Dial Transplant. 2010, 25: 3026-3033. 10.1093/ndt/gfq196.

    CAS PubMed Article Google Scholar

  30. Terawaki H, Matsuyama Y, Matsuo N, Ogura M, Mitome J, Hamaguchi A, Terada T, Era S, Hosoya T: A lower level of reduced albumin induces serious cardiovascular incidence among peritoneal dialysis patients. Clin Exp Nephrol. 2012, 16: 629-635. 10.1007/s10157-012-0610-x.

    CAS PubMed Article Google Scholar


DOI: 10.1186

Published on: 20130107


Authors:

Hiroyuki Terawaki, Yoshimitsu Hayashi, Wan-Jun Zhu, Yukie Matsuyama, Tomoyoshi Terada, Shigeru Kabayama, Tsuyoshi Watanabe, Seiichi Era, Bunpei Sato & Masaaki Nakayama

Transperitoneal administration of dissolved hydrogen for peritoneal dialysis patients: a novel approach to suppress oxidative stress in the peritoneal cavity

https://medicalgasresearch.biomedcentral.com/articles/10.1186/2045-9912-3-14

Abstract

Background

Oxidative stress (OS) associated with glucose breakdown products such as methylglyoxal has been reported to be associated with worsening peritoneal function in patients treated with peritoneal dialysis (PD). However, the use of antioxidants in general is limited due to their deleterious effects. This study aimed to elucidate the effects of a novel antioxidant molecular hydrogen (H2) on peritoneal OS using albumin redox status as a marker.

Methods

Effluent and blood samples from 6 normal PD patients were obtained during peritoneal equilibration testing using standard dialysate and hydrogen-rich dialysate. Determination of the redox state of albumin in wastewater and blood using high performance liquid chromatography.

Results

The H2-enriched dialysate (62.31 ± 11.10%) had significantly higher mean fractions of reduced albumin (ƒ(HMA)) in the effluent than the standard dialysate (54.70 ± 13.08%). Likewise, serum ƒ(HMA) was significantly higher in hydrogen-rich dialysate (65.75 ± 7.52%) than in standard dialysate (62.44 ± 7.66%).

Conclusion

Intraperitoneal administration of H2 reduces peritoneal and systemic OS.

References

  1. Yamamoto R, Otsuka Y, Nakayama M, Maruyama Y, Katoh N, Ikeda M, Yamamoto H, Yokoyama K, Kawaguchi Y, Matsushima M: Risk factors for encapsulating peritoneal sclerosis in patients who have experienced peritoneal dialysis treatment. Clin Exp Nephrol. 2005, 9: 148-152. 10.1007/s10157-005-0349-8.

    PubMed Article Google Scholar

  2. Kawaguchi Y, Ishizaki T, Imada A, Oohira S, Kuriyama S, Nakamoto H, Nakamoto M, Hiramatsu M, Maeda K, Ota K: Study Group for Withdrawal from PD in Japan: Searching for the reasons for drop-out from peritoneal dialysis: a nationwide survey in Japan. Perit Dial Int. 2003, 23 (Suppl 2): S175-177.

    PubMed Google Scholar

  3. Glomb MA, Monnier VM: Mechanism of protein modification by glyoxal and glycoaldehyde, reactive intermediates of the Maillard reaction. J Biol Cham. 1995, 270: 10017-10026. 10.1074/jbc.270.17.10017.

    CAS Article Google Scholar

  4. Nakayama M, Saito K, Sato E, Nakayama K, Terawaki H, Ito S, Kohno M: Radical generation by the non-enzymatic reaction of methylglyoxal and hydrogen peroxide. Redox Rep. 2007, 12: 125-133. 10.1179/135100007X200182.

    CAS PubMed Article Google Scholar

  5. Terawaki H, Nakao M, Nakayama K, Nakayama M, Kimura A, Takane K, Mitome J, Hamaguchi A, Ogura M, Yokoyama K, Ito S, Hosoya T: Peritoneal clearance and transport of methylglyoxal. Nephrol Dial Transplant. 2011, 26: 753-754. 10.1093/ndt/gfq698.

    PubMed Article Google Scholar

  6. Kawanishi H, Nakayama M, Miyazaki M, Honda K, Tomo T, Kasai K, Nakamoto H: NEXT-PD Study Group: Prospective multicenter observational study of encapsulating peritoneal sclerosis with neutral dialysis solution – the NEXT-PD study. Adv Perit Dial. 2010, 26: 71-74.

    PubMed Google Scholar

  7. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S: Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med. 2007, 13: 688-694. 10.1038/nm1577.

    CAS PubMed Article Google Scholar

  8. Abraini JH, Gardette-Chauffour MC, Martinez E, Rostain JC, Lemaire C: Psychophysiological reactions in humans during an open sea dive to 500 m with a hydrogen-helium-oxygen mixture. J Appl Physiol. 1994, 76: 1113-1118.

    CAS PubMed Google Scholar

  9. Fontanari P, Badier M, Guillot C, Tomei C, Burnet H, Gardette B, Jammes Y: Changes in maximal performance of inspiratory and skeletal muscles during and after the 7.1-MPa Hydra 10 record human dive. Eur J Appl Physiol. 2000, 81: 325-328. 10.1007/s004210050050.

    CAS PubMed Article Google Scholar

  10. Ohta S: Recent progress toward hydrogen medicine: potential of molecular hydrogen for preventive and therapeutic applications. Curr Pharm Des. 2011, 17: 2241-52. 10.2174/138161211797052664.

    CAS PubMed Central PubMed Article Google Scholar

  11. Abe T, Li XK, Yazawa K, Hatayama N, Xie L, Sato B, Kakuta Y, Tsutahara K, Okumi M, Tsuda H, Kaimori JY, Isaka Y, Natori M, Takahara S, Nonomura N: Hydrogen-rich University of Wisconsin solution attenuates renal cold ischemia-reperfusion injury. Transplantation. 2012, 94: 14-21.

    CAS PubMed Article Google Scholar

  12. American Heart Association: Criteria for the evaluation of the severity of established renal disease: Report of the council on the kidney in cardiovascular diseases. Circulation. 1971, 44: 306-307.

    Article Google Scholar

  13. Twardowski ZJ: PET-a simpler approach for determining prescriptions for adequate dialysis therapy. Adv Perit Dial. 1990, 6: 186-191.

    CAS PubMed Google Scholar

  14. Terawaki H, Takada Y, Era S, Funakoshi Y, Nakayama K, Nakayama M, Ogura M, Ito S, Hosoya T: The redox state of albumin and serious cardiovascular incidence in hemodialysis patients. Ther Apher Dial. 2010, 14: 465-471. 10.1111/j.1744-9987.2010.00841.x.

    PubMed Article Google Scholar

  15. Ishibashi Y, Sugimoto T, Ichikawa Y, Akatsuka A, Miyata T, Nangaku M, Tagawa H, Kurokawa K: Glucose dialysate induces mitochondrial DNA damage in peritoneal mesothelial cells. Perit Dial Int. 2002, 22: 11-21.

    PubMed Google Scholar

  16. Lee HB, Yu MR, Song JS, Ha H: Reactive oxygen species amplify protein kinase C signaling in high glucose-induced fibronectin expression by human peritoneal mesothelial cells. Kidney Int. 2004, 65: 1170-1179. 10.1111/j.1523-1755.2004.00491.x.

    CAS PubMed Article Google Scholar

  17. Gunal AI, Celiker H, Ustundag B, Akpolat N, Dogukan A, Akcicek F: The effect of oxidative stress inhibition with trimetazidine on the peritoneal alterations induced by hypertonic peritoneal dialysis solution. J Nephrol. 2003, 16: 225-230.

    CAS PubMed Google Scholar

  18. Shi P, Sun W, Shi P: A hypothesis on chemical mechanism of the effect of hydrogen. Med Gas Res. 2012, 2: 17-10.1186/2045-9912-2-17.

    CAS PubMed Central PubMed Article Google Scholar

  19. Ohsawa I, Nishimaki K, Yamagata K, Ishikawa M, Ohta S: Consumption of hydrogen water prevents atherosclerosis in apolipoprotein E knockout mice. Biochem Biophys Res Commun. 2008, 377: 1195-1198. 10.1016/j.bbrc.2008.10.156.

    CAS PubMed Article Google Scholar

  20. Sato Y, Kajiyama S, Amano A, Kondo Y, Sasaki T, Handa S, Takahashi R, Fukui M, Hasegawa G, Nakamura N, Fujinawa H, Mori T, Ohta M, Obayashi H, Maruyama N, Ishigami A: Hydrogen-rich pure water prevents superoxide formation in brain slices of vitamin C-depleted SMP30/GNL knockout mice. Biochem Biophys Res Commun. 2008, 375: 346-350. 10.1016/j.bbrc.2008.08.020.

    CAS PubMed Article Google Scholar

  21. Nakashima-Kamimura N, Mori T, Ohsawa I, Asoh S, Ohta S: Molecular hydrogen alleviates nephrotoxicity induced by anti-cancer drug cisplatin without compromising anti-tumor activity in mice. Cancer Chemother Pharmacol. 2009, 64: 753-761. 10.1007/s00280-008-0924-2.

    CAS PubMed Article Google Scholar

  22. Cardinal JS, Zhan J, Wang Y, Sugimoto R, Tsung A, McCurry KR, Billar TR, Nakao A: Oral hydrogen water prevents chronic allograft nephropathy in rats. Kidney Int. 2010, 77: 101-109. 10.1038/ki.2009.421.

    CAS PubMed Article Google Scholar

  23. Zhu WJ, Nakayama M, Mori T, Nakayama K, Katoh J, Murata Y, Sato T, Kabayama S, Ito S: Intake of water with high levels of dissolved hydrogen (H2) suppresses ischemia-induced cardio-renal injury in Dahl salt-sensitive rats. Nephrol Dial Transplant. 2011, 26: 2112-2118. 10.1093/ndt/gfq727.

    CAS PubMed Article Google Scholar

  24. Kajiyama S, Hasegawa G, Asano M, Hosoda H, Fukui M, Nakamura N, Kitawaki J, Imai S, Nakano K, Ohta M, Adachi T, Obayashi H, Yoshikawa T: Supplementation of hydrogen-rich water improves lipid and glucose metabolism in patients with type 2 diabetes or impaired glucose tolerance. Nutr Res. 2008, 28: 137-143. 10.1016/j.nutres.2008.01.008.

    CAS PubMed Article Google Scholar

  25. Nakao A, Toyoda Y, Sharma P, Evans M, Guthrie N: Effectiveness of hydrogen rich water on antioxidant status of subjects with potential metabolic syndrome – an open label pilot study. J Clin Biochem Nutr. 2010, 46: 140-149. 10.3164/jcbn.09-100.

    PubMed Central PubMed Article Google Scholar

  26. Ito M, Ibi T, Sahashi K, Ichihara M, Ito M, Ohno K: Open-label trial and randomized, double-blind, placebo-controlled crossover trial of hydrogen-enriched water for mitochondrial and inflammatory myopathies. Med Gas Res. 2011, 1: 24-10.1186/2045-9912-1-24.

    CAS PubMed Central PubMed Article Google Scholar

  27. Ishibashi T, Sato B, Rikitake M, Seo T, Kurokawa R, Hara Y, Naritomi Y, Hara H, Nagao T: Consumption of water containing a high concentration of molecular hydrogen reduces oxidative stress and disease activity in patients with rheumatoid arthritis: an open-label pilot study. Med Gas Res. 2012, 2: 27-10.1186/2045-9912-2-27.

    CAS PubMed Central PubMed Article Google Scholar

  28. Nakayama M, Kabayama S, Nakano H, Zhu WJ, Terawaki H, Nakayama K, Katoh K, Satoh T, Ito S: Biological effect of electrolyzed water in hemodialysis. Nephron Clin Pract. 2009, 112: c9-15. 10.1159/000210569.

    CAS PubMed Article Google Scholar

  29. Nakayama M, Nakano H, Hamada H, Itami N, Nakazawa R, Ito S: A novel bioactive haemodialysis system using dissolved dihydrogen (H2) produced by water electrolysis: a clinical trial. Nephrol Dial Transplant. 2010, 25: 3026-3033. 10.1093/ndt/gfq196.

    CAS PubMed Article Google Scholar

  30. Terawaki H, Matsuyama Y, Matsuo N, Ogura M, Mitome J, Hamaguchi A, Terada T, Era S, Hosoya T: A lower level of reduced albumin induces serious cardiovascular incidence among peritoneal dialysis patients. Clin Exp Nephrol. 2012, 16: 629-635. 10.1007/s10157-012-0610-x.

    CAS PubMed Article Google Scholar

References