Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 545467, 7 pages
http://dx.doi.org/10.1155/2015/545467
Review Article

Glutamine: An Obligatory Parenteral Nutrition Substrate in Critical Care Therapy

Department of Nutrition and Food Sciences, University of Bonn, 53115 Bonn, Germany

Received 31 July 2015; Accepted 16 September 2015

Academic Editor: Gisele P. De Oliveira

Copyright © 2015 Peter Stehle and Katharina S. Kuhn. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Roth, “Nonnutritive effects of glutamine,” Journal of Nutrition, vol. 138, no. 10, pp. 2025S–2031S, 2008. View at Google Scholar · View at Scopus
  2. P. Newsholme, J. Procopio, M. M. Ramos Lima, T. C. Pithon-Curi, and R. Curi, “Glutamine and glutamate—their central role in cell metabolism and function,” Cell Biochemistry and Function, vol. 21, no. 1, pp. 1–9, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Curi, C. J. Lagranha, S. Q. Doi et al., “Molecular mechanisms of glutamine action,” Journal of Cellular Physiology, vol. 204, no. 2, pp. 392–401, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Bergstrom, P. Furst, L. O. Noree, and E. Vinnars, “Intracellular free amino acid concentration in human muscle tissue,” Journal of Applied Physiology, vol. 36, no. 6, pp. 693–697, 1974. View at Google Scholar · View at Scopus
  5. P. Fürst, “Intracellular muscle free amino acids—their measurement and function,” Proceedings of the Nutrition Society, vol. 42, no. 3, pp. 451–462, 1983. View at Publisher · View at Google Scholar · View at Scopus
  6. K. S. Kuhn, P. Stehle, and P. Fürst, “Quantitative analyses of glutamine in peptides and proteins,” Journal of Agricultural and Food Chemistry, vol. 44, no. 7, pp. 1808–1811, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. B. A. van Acker, M. F. von Meyenfeldt, R. R. van der Hulst et al., “Glutamine: the pivot of our nitrogen economy?” Journal of Parenteral & Enteral Nutrition, vol. 23, no. 5, supplement, pp. S45–S48, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Wernerman and E. Vinnars, “The effect of trauma and surgery on interorgan fluxes of amino acids in man,” Clinical Science, vol. 73, no. 2, pp. 129–133, 1987. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Fürst, B. Alteheld, and P. Stehle, “Why should a single nutrient—glutamine—improve outcome? The remarkable story of glutamine dipeptides,” Clinical Nutrition Supplements, vol. 1, no. 1, pp. 3–15, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Singer, G. S. Doig, and C. Pichard, “The truth about nutrition in the ICU,” Intensive Care Medicine, vol. 40, no. 2, pp. 252–255, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Singer, M. M. Berger, G. Van den Berghe et al., “ESPEN Guidelines on Parenteral Nutrition: intensive care,” Clinical Nutrition, vol. 28, no. 4, pp. 387–400, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. P. E. Wischmeyer, R. Dhaliwal, M. McCall, T. R. Ziegler, and D. K. Heyland, “Parenteral glutamine supplementation in critical illness: a systematic review,” Critical Care, vol. 18, no. 2, article R76, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Bollhalder, A. M. Pfeil, Y. Tomonaga, and M. Schwenkglenks, “A systematic literature review and meta-analysis of randomized clinical trials of parenteral glutamine supplementation,” Clinical Nutrition, vol. 32, no. 2, pp. 213–223, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. A. R. van Zanten, Z. Hofman, and D. K. Heyland, “Consequences of the REDOXS and METAPLUS trials: the end of an era of glutamine and antioxidant supplementation for critically ill patients?” Journal of Parenteral and Enteral Nutrition, 2015. View at Publisher · View at Google Scholar
  15. A. R. H. van Zanten, “Glutamine and antioxidants: status of their use in critical illness,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 18, no. 2, pp. 179–186, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Heyland, J. Muscedere, P. E. Wischmeyer et al., “A randomized trial of glutamine and antioxidants in critically Ill patients,” The New England Journal of Medicine, vol. 368, no. 16, pp. 1489–1497, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Heyland, P. Wischmeyer, J. Muscedere et al., “The efffect of high-dose glutamine and antioxidant supplementation in critically ill patients: secondary subgroup analysis of the REDOXS trial,” ASPEN Clinical Nutrition Week, Article ID P1517432, 2013. View at Google Scholar
  18. D. K. Heyland, G. Elke, D. Cook et al., “Glutamine and antioxidants in the critically ill patient: a post hoc analysis of a large-scale randomized trial,” Journal of Parenteral & Enteral Nutrition, vol. 39, no. 4, pp. 401–409, 2015. View at Publisher · View at Google Scholar
  19. E. Vinnars, J. Bergstom, and P. Furst, “Influence of the postoperative state on the intracellular free amino acids in human muscle tissue,” Annals of Surgery, vol. 182, no. 6, pp. 665–671, 1975. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Askanazi, D. H. Elwyn, J. M. Kinney et al., “Muscle and plasma amino acids after injury: the role of inactivity,” Annals of Surgery, vol. 188, no. 6, pp. 797–803, 1978. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Askanazi, Y. A. Carpentier, C. B. Michelsen et al., “Muscle and plasma amino acids following injury. Influence of intercurrent infection,” Annals of Surgery, vol. 192, no. 1, pp. 78–85, 1980. View at Publisher · View at Google Scholar · View at Scopus
  22. J. M. Engel, J. Mühling, S. Weiss et al., “Low plasma glutamine after multiple trauma: relationship with intracellular glutamine in polymorphonuclear neutrophils during prolonged ICU stay,” Acta Anaesthesiologica Scandinavica, vol. 47, no. 6, pp. 707–713, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Gamrin, P. Essén, A. M. Forsberg, E. Hultman, and J. Wernerman, “A descriptive study of skeletal muscle metabolism in critically ill patients: Free amino acids, energy-rich phosphates, protein, nucleic acids, fat, water, and electrolytes,” Critical Care Medicine, vol. 24, no. 4, pp. 575–583, 1996. View at Publisher · View at Google Scholar · View at Scopus
  24. F. Hammarqvist, J.-L. Luo, I. A. Cotgreave, K. Andersson, and J. Wernerman, “Skeletal muscle glutathione is depleted in critically ill patients,” Critical Care Medicine, vol. 25, no. 1, pp. 78–84, 1997. View at Publisher · View at Google Scholar · View at Scopus
  25. D. C. Gore and R. R. Wolfe, “Metabolic response of muscle to alanine, glutamine, and valine supplementation during severe illness,” Journal of Parenteral & Enteral Nutrition, vol. 27, no. 5, pp. 307–314, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Mittendorfer, D. C. Gore, D. N. Herndon, and R. R. Wolfe, “Accelerated glutamine synthesis in critically ill patients cannot maintain normal intramuscular free glutamine concentration,” Journal of Parenteral and Enteral Nutrition, vol. 23, no. 5, pp. 243–252, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Biolo, R. Y. D. Flemming, S. P. Maggi, T. T. Nguyen, D. N. Herndon, and R. R. Wolfe, “Inhibition of muscle glutamine formation in hypercatabolic patients,” Clinical Science, vol. 99, no. 3, pp. 189–194, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Roth, G. Zoch, W. Mauritz et al., “Metabolic changes of patients with acute necrotizing pancreatitis,” Infusionstherapie und Klinische Ernährung, vol. 13, no. 4, pp. 172–179, 1986. View at Google Scholar · View at Scopus
  29. R. D. Griffiths, C. Jones, and T. E. A. Palmer, “Six-month outcome of critically ill patients given glutamine-supplemented parenteral nutrition,” Nutrition, vol. 13, no. 4, pp. 295–302, 1997. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Jones, T. E. Allan Palmer, and R. D. Griffiths, “Randomized clinical outcome study of critically ill patients given glutamine-supplemented enteral nutrition,” Nutrition, vol. 15, no. 2, pp. 108–115, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Goeters, A. Wenn, N. Mertes et al., “Parenteral L-alanyl-L-glutamine improves 6-month outcome in critically ill patients,” Critical Care Medicine, vol. 30, no. 9, pp. 2032–2037, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. G. L. Jensen, R. H. Miller, D. G. Talabiska, J. Fish, and L. Gianferante, “A double-blind, prospective, randomized study of glutamine-enriched compared with standard peptide-based feeding in critically ill patients,” The American Journal of Clinical Nutrition, vol. 64, no. 4, pp. 615–621, 1996. View at Google Scholar · View at Scopus
  33. A. P. J. Houdijk, E. R. Rijnsburger, J. Jansen et al., “Randomised trial of glutamine-enriched enteral nutrition on infectious morbidity in patients with multiple trauma,” The Lancet, vol. 352, no. 9130, pp. 772–776, 1998. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Roth, J. Funovics, F. Mühlbacher et al., “Metabolic disorders in severe abdominal sepsis: glutamine deficiency in skeletal muscle,” Clinical Nutrition, vol. 1, no. 1, pp. 25–41, 1982. View at Publisher · View at Google Scholar · View at Scopus
  35. W. Druml, G. Heinzel, and G. Kleinberger, “Amino acid kinetics in patients with sepsis,” American Journal of Clinical Nutrition, vol. 73, no. 5, pp. 908–913, 2001. View at Google Scholar · View at Scopus
  36. M. Parry-Billings, P. C. Calder, E. A. Newsholme, and J. Evans, “Does glutamine contribute to immunosuppression after major burns?” The Lancet, vol. 336, no. 8714, pp. 523–525, 1990. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Garrel, J. Patenaude, B. Nedelec et al., “Decreased mortality and infectious morbidity in adult burn patients given enteral glutamine supplements: a prospective, controlled, randomized clinical trial,” Critical Care Medicine, vol. 31, no. 10, pp. 2444–2449, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Stehle, J. Zander, N. Mertes et al., “Effect of parenteral glutamine peptide supplements on muscle glutamine loss and nitrogen balance after major surgery,” The Lancet, vol. 333, no. 8632, pp. 231–233, 1989. View at Publisher · View at Google Scholar · View at Scopus
  39. P. E. Wischmeyer, “Glutamine and heat shock protein expression,” Nutrition, vol. 18, no. 3, pp. 225–228, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. G. P. Oliveira, C. M. Dias, P. Pelosi, and P. R. M. Rocco, “Understanding the mechanisms of glutamine action in critically ill patients,” Anais da Academia Brasileira de Ciencias, vol. 82, no. 2, pp. 417–430, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. E. A. Newsholme, B. Crabtree, and M. S. M. Ardawi, “Glutamine metabolism in lymphocytes: its biochemical, physiological and clinical importance,” Quarterly Journal of Experimental Physiology, vol. 70, no. 4, pp. 473–489, 1985. View at Publisher · View at Google Scholar · View at Scopus
  42. E. A. Newsholme and P. C. Calder, “The proposed role of glutamine in some cells of the immune system and speculative consequences for the whole animal,” Nutrition, vol. 13, no. 7-8, pp. 728–730, 1997. View at Google Scholar · View at Scopus
  43. M. I. Amores-Sánchez and M. Á. Medina, “Glutamine, as a precursor of glutathione, and oxidative stress,” Molecular Genetics and Metabolism, vol. 67, no. 2, pp. 100–105, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Cöeffier, R. Marion-Letellier, and P. Déchelotte, “Potential for amino acids supplementation during inflammatory bowel diseases,” Inflammatory Bowel Diseases, vol. 16, no. 3, pp. 518–524, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. P. E. Wischmeyer, “Clinical applications of L-glutamine: past, present, and future,” Nutrition in Clinical Practice, vol. 18, no. 5, pp. 377–385, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Schlemmer, U. Suchner, B. Schapers et al., “Is glutamine deficiency the link between inflammation, malnutrition, and fatigue in cancer patients?” Clinical Nutrition, 2015. View at Publisher · View at Google Scholar
  47. P. Newsholme, “Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection?” Journal of Nutrition, vol. 131, no. 9, supplement, pp. 2515S–2522S, 2001. View at Google Scholar · View at Scopus
  48. G. Biolo, F. Zorat, R. Antonione, and B. Ciocchi, “Muscle glutamine depletion in the intensive care unit,” International Journal of Biochemistry and Cell Biology, vol. 37, no. 10, pp. 2169–2179, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. J. M. Lacey and D. W. Wilmore, “Is glutamine a conditionally essential amino acid?” Nutrition Reviews, vol. 48, no. 8, pp. 297–309, 1990. View at Google Scholar · View at Scopus
  50. P. Fürst and P. Stehle, “What are the essential elements needed for the determination of amino acid requirements in humans?” Journal of Nutrition, vol. 134, no. 6, supplement, pp. 1558S–1565S, 2004. View at Google Scholar · View at Scopus
  51. P. Fürst, “New developments in glutamine delivery,” Journal of Nutrition, vol. 131, no. 9, supplement, pp. 2562S–2568S, 2001. View at Google Scholar · View at Scopus
  52. S. Albers, J. Wernerman, P. Stehle, E. Vinnars, and P. Fürst, “Availability of amino acids supplied intravenously in healthy man as synthetic dipeptides: kinetic evaluation of L-alanyl-L-glutamine and glycyl-L-tyrosine,” Clinical Science, vol. 75, no. 5, pp. 463–468, 1988. View at Publisher · View at Google Scholar · View at Scopus
  53. D. E. Matthews, A. Battezzati, and P. Fürst, “Alanylglutamine kinetics in humans,” Clinical Nutrition, vol. 12, no. 1, pp. 57–58, 1993. View at Publisher · View at Google Scholar · View at Scopus
  54. P. Fürst, S. Albers, and P. Stehle, “Availability of glutamine supplied intravenously as alanylglutamine,” Metabolism, vol. 38, no. 8, supplement 1, pp. 67–72, 1989. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Albers, J. Wernerman, P. Stehle, E. Vinnars, and P. Fürst, “Availability of amino acids supplied by constant intravenous infusion of synthetic dipeptides in healthy man,” Clinical Science, vol. 76, no. 6, pp. 643–648, 1989. View at Publisher · View at Google Scholar · View at Scopus
  56. W. Druml, “Protein metabolism in acute renal failure,” Mineral and Electrolyte Metabolism, vol. 24, no. 1, pp. 47–54, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Duška, M. Fric, J. Pažout, P. Waldauf, P. Tůma, and J. Pachl, “Frequent intravenous pulses of growth hormone together with alanylglutamine supplementation in prolonged critical illness after multiple trauma: effects on glucose control, plasma IGF-I and glutamine,” Growth Hormone and IGF Research, vol. 18, no. 1, pp. 82–87, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. F. Duška, M. Fric, P. Waldauf et al., “Frequent intravenous pulses of growth hormone together with glutamine supplementation in prolonged critical illness after multiple trauma: effects on nitrogen balance, insulin resistance, and substrate oxidation,” Critical Care Medicine, vol. 36, no. 6, pp. 1707–1713, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. T. R. Ziegler, L. G. Ogden, K. D. Singleton et al., “Parenteral glutamine increases serum heat shock protein 70 in critically ill patients,” Intensive Care Medicine, vol. 31, no. 8, pp. 1079–1086, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. Y.-P. Zhou, Z.-M. Jiang, Y.-H. Sun, G.-Z. He, and H. Shu, “The effects of supplemental glutamine dipeptide on gut integrity and clinical outcome after major escharectomy in severe burns: a randomized, double-blind, controlled clinical trial,” Clinical Nutrition, Supplement, vol. 1, no. 1, pp. 55–60, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. P. Déchelotte, M. Hasselmann, L. Cynober et al., “L-alanyl-L-glutamine dipeptide-supplemented total parenteral nutrition reduces infectious complications and glucose intolerance in critically ill patients: the French controlled, randomized, double-blind, multicenter study,” Critical Care Medicine, vol. 34, no. 3, pp. 598–604, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Grau, A. Bonet, E. Miñambres et al., “The effect of L-alanyl-L-glutamine dipeptide supplemented total parenteral nutrition on infectious morbidity and insulin sensitivity in critically ill patients,” Critical Care Medicine, vol. 39, no. 6, pp. 1263–1268, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Fuentes-Orozco, R. Anaya-Prado, A. González-Ojeda et al., “L-alanyl-L-glutamine-supplemented parenteral nutrition improves infectious morbidity in secondary peritonitis,” Clinical Nutrition, vol. 23, no. 1, pp. 13–21, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. C. F. Estívariz, D. P. Griffith, M. Luo et al., “Efficacy of parenteral nutrition supplemented with glutamine dipeptide to decrease hospital infections in critically ill surgical patients,” Journal of Parenteral and Enteral Nutrition, vol. 32, no. 4, pp. 389–402, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Fuentes-Orozco, G. Cervantes-Guevara, I. Muciño-Hernández et al., “L-alanyl-L-glutamine-supplemented parenteral nutrition decreases infectious morbidity rate in patients with severe acute pancreatitis,” Journal of Parenteral and Enteral Nutrition, vol. 32, no. 4, pp. 403–411, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. X.-L. He, Q.-J. Ma, J.-G. Lu, Y.-K. Chu, and X.-L. Du, “Effect of total parenteral nutrition (TPN) with and without glutamine dipeptide supplementation on outcome in severe acute pancreatitis (SAP),” Clinical Nutrition Supplements, vol. 1, no. 1, pp. 43–47, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. I. M. Grintescu, I. L. Vasiliu, I. C. Badica et al., “The influence of parenteral glutamine supplementation on glucose homeostasis in critically ill polytrauma patients—a randomized-controlled clinical study,” Clinical Nutrition, vol. 34, no. 3, pp. 377–382, 2015. View at Publisher · View at Google Scholar · View at Scopus
  68. G. Cai, J. Yan, Z. Zhang, and Y. Yu, “Immunomodulatory effects of glutamine-enriched nutritional support in elderly patients with severe sepsis: a prospective, randomized, controlled study,” Journal of Organ Dysfunction, vol. 4, no. 1, pp. 31–37, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Şahin, S. M. MercanlIgil, N. Inanç, and E. Ok, “Effects of glutamine-enriched total parenteral nutrition on acute pancreatitis,” European Journal of Clinical Nutrition, vol. 61, no. 12, pp. 1429–1434, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. K. M. Tao, X. Q. Li, L. Q. Yang et al., “Glutamine supplementation for critically ill adults,” Cochrane Database of Systematic Reviews, vol. 9, Article ID CD010050, 2014. View at Publisher · View at Google Scholar
  71. M. C. Reade, A. Delaney, M. J. Bailey, and D. C. Angus, “Bench-to-bedside review: avoiding pitfalls in critical care meta-analysis—funnel plots, risk estimates, types of heterogeneity, baseline risk and the ecologic fallacy,” Critical Care, vol. 12, no. 4, article 220, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. I. K. Crombie and H. T. O. Davies, What is Meta-Analysis?Hayward, 2nd edition, 2009.
  73. L. Pradelli, S. Iannazzo, O. Zaniolo, M. Muscaritoli, and M. Eandi, “Effectiveness and cost-effectiveness of supplemental glutamine dipeptide in total parenteral nutrition therapy for critically ill patients: a discrete event simulation model based on Italian data,” International Journal of Technology Assessment in Health Care, vol. 28, no. 1, pp. 22–28, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. L. Pradelli, M. Povero, M. Muscaritoli, and M. Eandi, “Updated cost-effectiveness analysis of supplemental glutamine for parenteral nutrition of intensive-care patients,” European Journal of Clinical Nutrition, vol. 69, no. 5, pp. 546–551, 2015. View at Publisher · View at Google Scholar · View at Scopus
  75. P. Wischmeyer, “Glutamine supplementation in parenteral nutrition and intensive care unit patients: are we throwing the baby out with the bathwater?” Journal of Parenteral & Enteral Nutrition, 2015. View at Publisher · View at Google Scholar
  76. P. Fürst and P. Stehle, “Are intravenous amino acid solutions unbalanced?” New Horizons, vol. 2, no. 2, pp. 215–223, 1994. View at Google Scholar · View at Scopus
  77. S. A. McClave, R. G. Martindale, T. W. Rice, and D. K. Heyland, “Feeding the critically ill patient,” Critical Care Medicine, vol. 42, no. 12, pp. 2600–2610, 2014. View at Publisher · View at Google Scholar · View at Scopus
  78. P. Newsholme, M. M. R. Lima, J. Procopio et al., “Glutamine and glutamate as vital metabolites,” Brazilian Journal of Medical and Biological Research, vol. 36, no. 2, pp. 153–163, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Stumvoll, C. Meyer, G. Perriello, M. Kreider, S. Welle, and J. Gerich, “Human kidney and liver gluconeogenesis: evidence for organ substrate selectivity,” American Journal of Physiology—Endocrinology and Metabolism, vol. 274, no. 5, part 1, pp. E817–E826, 1998. View at Google Scholar · View at Scopus
  80. KDIGO, “KDIGO clinical practice guideline for acute kidney injury,” Kidney International Supplements, vol. 2, pp. 8–12, 2012. View at Google Scholar
  81. X. Wei, A. G. Day, H. Ouellette-Kuntz, and D. K. Heyland, “The association between nutritional adequacy and long-term outcomes in critically ill patients requiring prolonged mechanical ventilation: a multicenter cohort study,” Critical Care Medicine, vol. 43, no. 8, pp. 1569–1579, 2015. View at Publisher · View at Google Scholar