Advertisement
Original article| Volume 131, ISSUE 5, P447-455, May 1998

Download started.

Ok

Beneficial effects of chronic administration of dietary ω-3 polyunsaturated fatty acids in dogs with renal insufficiency

  • Scott A. Brown
    Correspondence
    Reprint requests: Dr. Scott A. Brown, Department of Physiology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.
    Affiliations
    Department of Physiology and Pharmacology and the Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA

    Mark Morris Associates, Topeka, Kansas, USA
    Search for articles by this author
  • Cathy A. Brown
    Affiliations
    Department of Physiology and Pharmacology and the Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA

    Mark Morris Associates, Topeka, Kansas, USA
    Search for articles by this author
  • Wayne A. Crowell
    Affiliations
    Department of Physiology and Pharmacology and the Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA

    Mark Morris Associates, Topeka, Kansas, USA
    Search for articles by this author
  • Jeanne A. Barsanti
    Affiliations
    Department of Physiology and Pharmacology and the Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA

    Mark Morris Associates, Topeka, Kansas, USA
    Search for articles by this author
  • Timothy Allen
    Affiliations
    Department of Physiology and Pharmacology and the Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA

    Mark Morris Associates, Topeka, Kansas, USA
    Search for articles by this author
  • Christopher Cowell
    Affiliations
    Department of Physiology and Pharmacology and the Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA

    Mark Morris Associates, Topeka, Kansas, USA
    Search for articles by this author
  • Delmar R. Finco
    Affiliations
    Department of Physiology and Pharmacology and the Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA

    Mark Morris Associates, Topeka, Kansas, USA
    Search for articles by this author
      This paper is only available as a PDF. To read, Please Download here.

      Abstract

      Dietary supplementation with polyunsaturated fatty acids (PUFA) alters the course of experimental renal disease in rats. However, chronic renal disease in other laboratory animals and in human beings frequently responds differently to experimental manipulations. We investigated the effects of variations in dietary PUFA composition on the chronic course of induced renal disease in dogs. Two months after Math Eq nephrectomy, dogs were randomly divided into three groups of seven animals each. For the next 20 months, each group of dogs was fed a low-fat basal diet supplemented with one of three sources of lipid to achieve a final concentration of 15% added fat. Fat sources provided ω-3 PUFA (menhaden fish oil, group FO), ω-6 PUFA (safflower oil, group SO), or saturated fatty acids (beef tallow, group BT). Throughout the dietary trial, the magnitude of proteinuria and the plasma concentrations of creatinine, cholesterol, and triglyceride were lower in group FO. The mean overall glomerular filtration rate was 0.89 ± 0.18 ml/min per kilogram of body weight in group SO, a value that was significantly less (p < 0.05) than the corresponding values for groups BT and FO (1.21 ± 0.18 and 1.43 ± 0.20 ml/min/kg, respectively). Renal interstitial fibrosis also was significantly elevated in group SO. The extents of mesangial matrix expansion, glomerulosclerosis, and renal interstitial cellular infiltrate were similar in groups BT and SO, but lower (p < 0.05) in group FO. We conclude that supplementation with ω-6 PUFA enhanced renal injury; supplementation with ω-3 PUFA was renoprotective.

      Abbreviations:

      BT (Beef tallow), BUN (blood urea nitrogen), CCr (urinary clearance of exogenously administered creatinine), FO (menhaden fish oil), GFR (glomerular filtration rate), HDLcholesterol (cholesterol contained in high-density lipoprotein particles), PAS (periodic acidSchiff), PUFA (polyunsaturated fatty acids), SCr (serum creatinine concentration), SO (safflower oil)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Translational Research
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Barcelli U
        • Miyata J
        • Ito Y
        • et al.
        Beneficial effects of polyunsaturated fatty acids in partially nephrectomized rats.
        Prostaglandins. 1986; 32: 211-219
        • Scharschmidt LA
        • Gibbons NB
        • McGarry L
        • et al.
        Effects of dietary fish oil on renal insufficiency in rats with subtotal nephrectomy.
        Kidney Int. 1987; 32: 700-709
        • Clark WF
        • Parbtani A
        • Philbrick DJ
        • Holub BJ
        • Huff MW
        Chronic effects of omega-3 fatty acids (fish oil) in a rat Math Eq renal ablation model.
        J Am Soc Nephrol. 1991; 1: 1343-1353
        • Logan JL
        • Michael UF
        • Benson B
        Dietary fish oil interferes with renal arachidonic acid metabolism in rats: correlation with renal physiology.
        Metabolism. 1992; 41: 382-389
        • Donadio JV
        • Bergstralh EJ
        • Offord KP
        • Spencer DC
        • Holley KE
        A controlled trial of fish oil in IgA nephropathy.
        N Engl J Med. 1994; 331: 1194-1199
        • Homan JJ
        • Biol HJ
        • Donker AJ
        • Wilmink JM
        • Sluiter WJ
        • Tegzess AM
        The effects of dietary supplementation with fish oil on renal function and the course of early postoperative rejection episodes in cyclosporine-treated renal transplant recipients.
        Transplantation. 1992; 54: 257-263
        • Clark WF
        • Parabtani A
        • Naylor CD
        • et al.
        Fish oil in lupus nephritis: clinical findings and methodological implications.
        Kidney Int. 1993; 44: 75-86
        • Polzin DL
        • Leininger JR
        • Osborne CA
        • Jeraj K
        Development of renal lesions in dogs after Math Eq reduction of renal mass.
        Lab Invest. 1988; 58: 172-183
        • Brown SA
        • Crowell WA
        • Barsanti JA
        • White JV
        • Finco DR
        Beneficial effects of dietary mineral restriction in dogs with marked reduction of functional renal mass.
        J Am Soc Nephrol. 1991; 1: 1169-1179
        • Brown SA
        • Finco DR
        • Crowell WA
        • Navar LG
        Dietary protein intake and the glomerular adaptations to partial nephrectomy in dogs.
        J Nutr. 1991; 121: S125-S127
        • Finco DR
        • Brown SA
        • Crowell WA
        • Duncan RJ
        • Barsanti JA
        • Bennett SE
        Effects of dietary phosphorus and protein in dogs with chronic renal failure.
        Am J Vet Res. 1992; 53: 2264-2271
        • Brown SA
        • Finco DR
        • Crowell WA
        • Choat DC
        • Navar LG
        Single-nephron adaptations to partial renal ablation in the dog.
        Am J Physiol. 1990; 258: F495-F503
        • Brown SA
        • Walton CA
        • Crawford P
        • Bakris GL
        Long-term effects of antihypertensive regimens on renal hemodynamics and proteinuria.
        Kidney Int. 1993; 43: 1210-1218
        • Bovee KC
        • Kronfeld DS
        • Ramberg C
        • Goldschmidt M
        Long-term measurement of renal function in partially nephrectomized dogs fed 56, 27, or 19% protein.
        Investig Urol (Berl). 1979; 16: 378-384
        • Robertson JL
        • Goldschmidt M
        • Kronfeld DS
        • Tomaszewski JE
        • Hill S
        • Bovee KC
        Long-term renal responses to high dietary protein in dogs with 75% nephrectomy.
        Kidney Int. 1986; 29: 511-519
        • Finco DR
        • Brown SA
        • Crowell WA
        • Barsanti JA
        Exogenous creatinine clearance as a measure of glomerular filtration rate in dogs with reduced renal mass.
        Am J Vet Res. 1991; 52: 1029-1032
        • Bradford MM
        A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
        Anal Biochem. 1976; 72: 248-254
        • Brown SA
        • Brown CA
        Single-nephron adaptations to partial renal ablation in cats.
        Am J Physiol. 1995; 269: R1002-R1008
        • Finco DR
        • Coulter DB
        • Barsanti JA
        Procedure for a simple method of measuring glomerular filtration rate in the dog.
        J Am Anim Hosp Assoc. 1982; 18: 804-806
        • Neumaryer HH
        • Heinrish M
        • Schmissas M
        • Haller H
        • Wagner K
        • Luft FC
        Amelioration of ischemic acute renal failure by dietary fish oil administration in conscious dogs.
        J Am Soc Nephrol. 1992; 3: 1312-1320
        • Abdel-Gayoum AA
        • Bashir AA
        • el-Fakhri MM
        Effects of fish oil and sunflower oil supplementation on gentamicininduced nephrotoxicity in rat.
        Hum Exp Toxicol. 1995; 14: 884-888
        • Kasiske BL
        • O'Donnell MP
        • Lee H
        • Kim Y
        • Keane WE
        Impact of dietary fatty acid supplementation on renal injury in obese Zucker rats.
        Kidney Int. 1991; 39: 1125-1134
        • Rahman MA
        • Sauter DC
        • Young MR
        Effects of fish oil on the induction of experimental membranous nephropathy in the rat.
        Lab Invest. 1991; 64: 371-376
        • Shimamura T
        • Wilson AC
        Influence of dietary fish oil on the aortic, myocardial, and renal lesions of SHR.
        J Nutr Sci Vitaminol (Tokyo). 1991; 37: 581-590
        • Wheeler DC
        • Nair DR
        • Persaud JW
        • et al.
        Effects of dietary fatty acids in an animal model of focal glomerulosclerosis.
        Kidney Int. 1991; 39: 930-937
        • Robinson DR
        • Xu LL
        • Tateno S
        • Guo M
        • Colvin RB
        Suppression of autoimmune disease by dietary n-3 fatty acids.
        J Lipid Res. 1993; 34: 1435-1444
        • Weise WJ
        • Natori Y
        • Levine JS
        • et al.
        Fish oil has protective and therapeutic effects on proteinuria in passive Heymann nephritis.
        Kidney Int. 1993; 43: 359-368
        • Chandrasekar B
        • Fernandes G
        Decreased pro-inflammatory cytokines and increased antioxidant enzyme gene expression by omega-3 lipids in murine lupus nephritis.
        Biochem Biophys Res Commun. 1994; 200: 893-898
        • Burgess NA
        • Reynolds TM
        • Williams N
        • Pathy A
        • Smith S
        Evaluation of four animal models of intrarenal calcium deposition and assessment of the influence of dietary supplementation with essential fatty acids on calcifications.
        Urol Res. 1995; 23: 239-242
        • Goldstein DJ
        • Wheeler DC
        • Sandstrom DJ
        • Kawachi H
        • Salant DJ
        Fish oil ameliorates renal injury and hyperlipidemia in the Milan normotensive rat model of focal glomerulosclerosis.
        J Am Soc Nephrol. 1995; 6: 1468-1475
        • Clark WF
        • Parbtani A
        • Philbrick DJ
        • Spanner E
        • Huff MW
        • Holub BJ
        Dietary protein restriction versus fish oil supplementation in the chronic remnant nephron model.
        Clin Nephrol. 1993; 39: 295-304
        • Aukema HM
        • Ogborn MR
        • Tomobe K
        • Takashi H
        • Hibino T
        • Holub BJ
        Effects of dietary protein restriction and oil type on the early progression of murine polycystic kidney disease.
        Kidney Int. 1992; 42: 837-842
        • Council NR
        Nutrient requirements of domestic animals: nutrient requirements of dogs.
        National Academy Press, Washington, DC1985
        • Clark WF
        • Parbtani A
        • Huff MW
        • Redi B
        • Holub BJ
        • Falardeau P
        Omega-3 fatty acid dietary supplementation in systemic lupus erythematosus.
        Kidney Int. 1989; 36: 653-660
        • Kaisiske B
        • O'Donnell M
        • Cleary M
        • Keane WE
        Treatment of hyperlipidemia reduces glomerular injury in obese Zucker rats.
        Kidney Int. 1988; 33: 662-667
        • Guijarno C
        • Keane WF
        Lipid-induced glomerular injury.
        Nephron. 1994; 67: 1-6
        • Keane WF
        • Kasiske BL
        • O'Donnell MP
        Hyperlipidemia and the progression of renal disease.
        Am J Clin Nutr. 1988; 47: 157-160
        • Wanner C
        • Kramer-Guth A
        • Nauck M
        • Quaschning T
        • Pavenstadt H
        • Schollmeyer P
        Cholesterol metabolism in glomerular cells: effect of lipoproteins from nephrotic patients.
        Miner Electrolyte Metab. 1996; 22: 39-46
        • Schmitz PG
        • O'Donnell MP
        • Kasiske BL
        • Keane WE
        Glomerular hemodynamic effects of dietary polyunsaturated fatty acid supplementation.
        J Lab Clin Med. 1991; 118: 129-135
        • Brenner BM
        • Meyer TW
        • Hostetter TH
        The role of hemodynamically mediated glomerular injury in the pathogenesis of progressive glomerular sclerosis in aging, renal ablation, and intrinsic renal disease.
        N Engl J Med. 1982; 307: 652-659
        • Hostetter TH
        • Olson JL
        • Rennke HG
        • Venkatachalam MA
        • Brenner BM
        Hyperfiltration in remnant nephrons: a potentially adverse response to renal ablation.
        Am J Physiol. 1981; 241: F85-F92
        • Dworkin LD
        • Benstein JA
        • Parker M
        • Tolbert E
        • Feiner HD
        Calcium antagonists and converting enzyme inhibitors reduce renal injury by different mechanisms.
        Kidney Int. 1993; 43: 808-814
        • Prickett JD
        • Robinson DW
        • Steinberg AD
        Effects of dietary enrichment with eicosapentaenoic acid upon autoimmune nephritis in female NZB X NZW/P1 mice.
        Arthritis Rheum. 1983; 26: 133-139
        • Donadio JV
        Omega-3 polyunsaturated fatty acids: a potential new treatment of immune renal disease.
        Mayo Clin Proc. 1991; 66: 1018-1028
        • Boutard V
        • Fouqueray B
        • Philippe C
        • Perez J
        • Baud L
        Fish oil supplementation and essential fatty acid deficiency reduce nitric oxide synthesis by rat macrophages.
        Kidney Int. 1994; 46: 1280-1286
        • Collie-Duguid ES
        • Wahale KW
        Inhibitory effect of fish oil n-3 polyunsaturated fatty acids on the expression of endothelial cell adhesion molecules.
        Biochem Biophys Res Commun. 1996; 220: 969-974
        • Barcelli U
        • Glass-Greenwalt P
        • Pollak VE
        Enhancing effects of dietary supplementation with omega-3 fatty acids on plasma fibrinolysis.
        Thromb Res. 1985; 39: 307-312
        • Clark WF
        • Parbtani A
        • Philbrick D
        • et al.
        Comparative efficacy of dietary treatments on renal function in rats with subtotal nephrectomy: renal polyunsaturated fatty acid incorporation and prostaglandin excretion.
        Clin Nephrol. 1990; 33: 25-34
        • Spurney RF
        • Ruiz P
        • Albrightson CR
        • Pisetsky DS
        • Coffman TM
        Fish oil feeding modulates leukotriene production in murine lupus nephritis.
        Prostaglandins. 1994; 48: 331-348
        • Chandrasekar B
        • Fernandes G
        Decreased pro-inflammatory cytokines and increased antioxidant enzyme gene expression by omega-3 lipids in murine nephritis.
        Biochem Biophys Res Commun. 1994; 200: 893-898
        • Radack K
        • Deck C
        • Huster G
        The effects of low doses of n3 fatty acid supplementation on blood pressure in hypertensive subjects.
        Arch Intern Med. 1991; 151: 1173-1180
        • Morris MC
        • Sacks F
        • Rosner B
        Does fish oil lower blood pressure?.
        Circulation. 1993; 88: 523-533
        • Mills DE
        • Ward RP
        • McCutcheon D
        • Dixon H
        • Ly H
        • Scholey J
        Attenuation of cyclosporine-induced hypertension by dietary fatty acids in the borderline hypertensive rat.
        Transplantation. 1992; 53: 649-654
        • Kimura S
        • Minami M
        • Saito H
        • Kobayashi T
        • Okuyama H
        Dietary docosahexaenoic acid (22: 6n-3) prevents the development of hypertension in SHRSP.
        Clin Exp Pharmacol Physiol. 1995; 22: S308-S309
        • Bidani A
        • Mitchell K
        • Schwartz MM
        • Navar LG
        • Lewis EJ
        Absence of glomerular injury or nephron loss in a normotensive rat remnant kidney model.
        Kidney Int. 1990; 38: 28-38
        • Panzetta O
        • Cominacini L
        • Garbin U
        • et al.
        Increased susceptibility of LDL to in vitro oxidation in patients on maintenance hemodialysis: effects of fish oil and vitamin E administration.
        Clin Nephrol. 1995; 44: 303-309