• 1.

    Petric AD, Stabej P, Zemva A. Dilated cardiomyopathy in Doberman Pinschers: survival, causes of death and a pedigree review in a related line. J Vet Cardiol 2002;4:1724.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Calvert CA, Pickus CW, Jacobs GJ, et al. Signalment, survival, and prognostic factors in Doberman Pinschers with end-stage cardiomyopathy. J Vet Intern Med 1997;11:323326.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Basso C, Fox PR, Meurs KM, et al. Arrhythmogenic right ventricular cardiomyopathy causing sudden cardiac death in boxer dogs: a new model of human disease. Circulation 2004;109:11801185.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Meurs KM, Spiers AW, Miller MW, et al. Familial ventricular arrhythmias in Boxers. J Vet Intern Med 1999;13:437439.

  • 5.

    Davila-Roman VG, Vedala G, Herrero P, et al. Altered myocardial fatty acid and glucose metabolism in idiopathic dilated cardiomyopathy. J Am Coll Cardiol 2002;40:271277.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Freeman LM, Rush JE, Kehayias JJ, et al. Nutritional alterations and the effect of fish oil supplementation in dogs with heart failure. J Vet Intern Med 1998;12:440448.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Smith CE, Freeman LM, Meydani M, et al. Myocardial concentrations of fatty acids in dogs with dilated cardiomyopathy. Am J Vet Res 2005;66:14831486.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Billman GE, Kang JX, Leaf A. Prevention of sudden cardiac death by dietary pure omega-3 polyunsaturated fatty acids in dogs. Circulation 1999;99:24522457.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Marchioli R, Barzi F, Bomba E, et al. Early protection against sudden death by n-3 polyunsaturated fatty acids after myocardial infarction: time-course analysis of the results of the Gruppo Italiano per lo Studio della Sopravivenza nell'Infarto Miocardico (GISSI)-Prevenzione. Circulation 2002;105:18971903.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Pepe S, McLennan PL. Dietary fish oil confers direct antiarrhythmic properties on the myocardium of rats. J Nutr 1996;126:3442.

  • 11.

    Smith CE, Freeman LM, Rush JE, et al. Omega-3 fatty acids in Boxer dogs with arrhythmogenic right ventricular cardiomyopathy. J Vet Intern Med 2007;21:265273.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911917.

  • 13.

    GISSI-Prevenzione Investigators. Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Lancet 1999;354:447455.

    • Search Google Scholar
    • Export Citation
  • 14.

    Albert CM, Campos H, Stampfer MJ, et al. Blood levels of longchain n-3 fatty acids and the risk of sudden death. New Engl J Med 2002;346:11131118.

  • 15.

    McLennan PL. Relative effects of dietary saturated, monounsaturated, and polyunsaturated fatty acids on cardiac arrhythmias in rats. Am J Clin Nutr 1993;57:207212.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Calvert CA, Hall G, Jacobs G, et al. Clinical and pathological findings in Doberman Pinschers with occult cardiomyopathy that died suddenly or developed congestive heart failure: 54 cases (1984–1991). J Am Vet Med Assoc 1997;210:505511.

    • Search Google Scholar
    • Export Citation
  • 17.

    Kraus MS, Moise NS, Rishniw M, et al. Morphology of ventricular arrhythmias in the boxer as measured by 12-lead electrocardiography with pace-mapping comparison. J Vet Intern Med 2002;16:153158.

    • Crossref
    • Search Google Scholar
    • Export Citation

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Plasma fatty acid concentrations in Boxers and Doberman Pinschers

Caren E. SmithDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA 01536.

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Lisa M. FreemanDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA 01536.

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Kathryn M. MeursDepartment of Veterinary Clinical Sciences, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210.

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John E. RushDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA 01536.

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Allison LambDepartment of Veterinary Clinical Sciences, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210.

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Abstract

Objective—To compare plasma fatty acid concentrations and the relationships of fatty acids to arrhythmias in Boxers versus Doberman Pinschers.

Animals—38 Boxers and 13 Doberman Pinschers.

Procedures—Boxers and Doberman Pinschers evaluated via Holter recording and for which a blood sample was available were included. Echocardiograms were performed in 49 of 51 dogs. The number of ventricular premature complexes (VPCs)/24 h was counted and fatty acids analyzed. Plasma fatty acid concentrations and VPCs/24 h, as well as correlations between the 2 variables, were compared between the 2 breeds.

Results—Compared with the Doberman Pinschers, Boxers had significantly higher plasma concentrations of γ-linolenic acid but lower concentrations of arachidonic acid. Total n-6 fatty acids and total polyunsaturated fatty acid concentrations were higher in Doberman Pinschers. There were significant, but weak, positive correlations between VPCs and oleic acid, total n-3 fatty acids, and total n-9 fatty acids in Boxers but not in Doberman Pinschers.

Conclusions and Clinical Relevance—Data suggested that plasma fatty acid concentrations may differ between Boxers and Doberman Pinschers and that the relationship between fatty acid concentrations and VPCs may be different between these 2 breeds.

Abstract

Objective—To compare plasma fatty acid concentrations and the relationships of fatty acids to arrhythmias in Boxers versus Doberman Pinschers.

Animals—38 Boxers and 13 Doberman Pinschers.

Procedures—Boxers and Doberman Pinschers evaluated via Holter recording and for which a blood sample was available were included. Echocardiograms were performed in 49 of 51 dogs. The number of ventricular premature complexes (VPCs)/24 h was counted and fatty acids analyzed. Plasma fatty acid concentrations and VPCs/24 h, as well as correlations between the 2 variables, were compared between the 2 breeds.

Results—Compared with the Doberman Pinschers, Boxers had significantly higher plasma concentrations of γ-linolenic acid but lower concentrations of arachidonic acid. Total n-6 fatty acids and total polyunsaturated fatty acid concentrations were higher in Doberman Pinschers. There were significant, but weak, positive correlations between VPCs and oleic acid, total n-3 fatty acids, and total n-9 fatty acids in Boxers but not in Doberman Pinschers.

Conclusions and Clinical Relevance—Data suggested that plasma fatty acid concentrations may differ between Boxers and Doberman Pinschers and that the relationship between fatty acid concentrations and VPCs may be different between these 2 breeds.

Boxers and Doberman Pinschers are frequently affected with cardiomyopathy, although the forms of the disease in these breeds (DCM or ARVC) may have somewhat different characteristics.1-3 Ventricular arrhythmias are common in both forms: DCM, primarily a left ventricular or biventricular disease, and ARVC, which primarily affects the right ventricle.1-3

Although genetic factors play an important role in cardiomyopathy and ventricular arrhythmias, another factor that may influence the disease is diet, particularly with regards to fat.1,4 Alterations in fatty acids are known to occur in cardiomyopathy and CHF. For example, the healthy adult heart uses long-chain fatty acids as its major energy source, but in CHF, the heart reverts to a fetal gene program and glucose is substituted for fatty acids as the myocardium's preferred oxidative substrate.5 Alterations in the individual types of fatty acids also occur. Decreased concentrations of the 2 major n-3 fatty acids, EPA and DHA, have been reported in dogs with CHF caused by DCM.6 A higher percentage of the n-6 fatty acid, docosatetraenoic acid, has been reported in the myocardial tissue of dogs with DCM, compared with healthy control dogs.7 Individual fatty acid type (eg, n-3 vs n-6 vs n-9) may also play a role in susceptibility to ventricular arrhythmia. For example, studies8-11 reveal that increasing plasma n-3 fatty acid concentrations through dietary supplementation or IV administration reduces arrhythmia number in humans, rodent and canine models of arrhythmia, and Boxers with naturally occurring ARVC.

Although relationships between arrhythmia and specific classes of fatty acids have been detected among various species, breed-specific differences in fatty acid concentrations and their relationships to arrhythmias in dogs have not been described. The goals of the study reported here were to compare plasma fatty acid concentrations in Boxers and Doberman Pinschers and determine whether correlations between frequency of VPC and individual plasma fatty acid concentrations exist in either or both of these breeds.

Materials and Methods

Boxers and Doberman Pinschers evaluated at The Ohio State University College of Veterinary Medicine between January 2003 and November 2004 were eligible for the study if they had been evaluated via 24-hour ambulatory electrocardiography and had a plasma sample available for analysis. All blood samples had been centrifuged, and the plasma was frozen at −80°C until analysis. Standard 2-dimensional, M-mode, and color flow Doppler echocardiography was performed.a A 3-channel transthoracic ambulatory electrocardiography system was attached to each dog for 25 hours.b A technician under the guidance of a veterinary cardiologist analyzed ambulatory electrocardiography recordings for the total number of VPCs/24 h by use of an analysis system.c Any dogs with recordings that did not have at least 20 hours of readable data were not included in the study. Dogs were considered to be affected by ARVC or DCM if they had > 100 VPCs/24 h or a fractional shortening of < 25%. Dogs receiving antiarrhythmic medications or fish oil supplements were excluded from analysis.

Lipid extraction—Total phospholipid fatty acids were analyzed.d Plasma lipids were extracted according to the method of Bligh and Dyer,12 whereby mixtures of plasma, methanol, chloroform, and water are prepared such that lipid is recovered in a chloroform layer. Trace amounts of butylated hydroxyl toluene (0.05%) were added to the chloroform to prevent oxidation of polyunsaturated fatty acids. The resulting lipid extracts were maintained under an atmosphere of nitrogen following extraction and kept frozen prior to additional processing.

Separation of lipid classes—Immediately prior to lipid class separation, lipid samples were dried under a gentle stream of nitrogen, rediluted in 50 mL of chloroform, and prepared for lipid class separation.

Lipid classes including total phospholipid, nonesterified fatty acids, triglyceride, and cholesterol esters were separated on commercial silica gel G plates.e The chromatographic plates were developed in a solvent system consisting of distilled petroleum ether (boiling point, 30° to 60°C):diethyl ether:acetic acid (80:20:1, by volume). Following development, the silica gel plates were sprayed with a methanolic solution containing 0.5% 2,7-dichlorofluorescein, which was used to visualize lipid classes under UV light. Desired corresponding lipid bands were scraped into screw-cap tubes. The samples were transesterified with boron trifluoride (12%) in methanolf in an 80°C water bath for 90 minutes. Resulting fatty acid methyl esters were extracted with water and petroleum ether and stored frozen at −80°C until gas chromatographic analysis was performed.

Fatty acid analysis—Lipid class fatty acid methyl ester composition was determined by use of capillary gas chromatography. Methyl ester samples were dessicated to dryness under nitrogen and resuspended in heptane containing methyl-tridecanoic acidg as an internal standard. Resulting fatty acid methyl esters were separated and quantified with a gas chromatographh by use of a 30-m free fatty acid–phase coating and commercial software.i The instrument temperature was programmed from 190° to 240°C at 7°C/min, with a final hold of 10 minutes, which separated and measured fatty acid methyl esters ranging from 12:0 to 24:1. The detector temperature was 250°C. Helium carrier gas was used at a flow rate of 1.4 mL/min and a split ratio of 1:25. Chromatographic data were collected and processed with commercial software.i Individual peaks, representing as little as 0.05% of the fatty acid methyl esters, were distinguished.

Fatty acids were identified by comparison to authentic fatty acid standards and quantitated with peak area and internal standard. Resulting data are expressed as percentage composition.

Statistical analysis—Data were examined graphically before analysis. All data are reported as median (range) for consistency because many of the fatty acid concentrations were not normally distributed. Data that were not normally distributed were transformed prior to analysis, and independent t tests were used to compare subject characteristics and plasma fatty acid concentrations between the 2 breeds, whereas Pearson correlations were used to compare individual plasma fatty acid concentrations with the number of VPCs/24 h. Commercial statistical software was used for analysis.j For all analyses, P < 0.05 was considered significant.

Results

Fifty-one dogs (38 Boxers and 13 Doberman Pinschers) were enrolled in the study (Table 1). Median age, sex, and number of VPCs/24 h were not significantly different between the 2 breeds. Echocardiograms were performed on 49 of 51 dogs. Two Doberman Pinschers and 1 Boxer had fractional shortening < 25% (P = 0.10). Seventeen dogs (13 Boxers and 4 Doberman Pinschers) were considered affected by either ARVC or DCM. Medications administered to the dogs included digoxin (1 Boxer), phenylpropanolamine (1 Boxer), phenobarbital (1 Boxer), and thyroxine (2 Boxers and 3 Doberman Pinschers). Some dogs were receiving more than 1 medication.

Table 1—

Signalment and plasma fatty acid concentrations (median [range]) of 38 Boxers and 13 Doberman Pinschers. Plasma fatty acid concentrations reported as percentage normalized values.

Table 1—

Compared with the Doberman Pinschers, Boxers had significantly (P < 0.001) higher plasma concentrations of γ-linolenic acid (C18:3W6) but had lower (P = 0.005) concentrations of arachidonic acid (C20:4 n-6;). Plasma concentrations of total polyunsaturated fatty acids (P < 0.001) and total n-6 fatty acids (P < 0.001) were higher in the Doberman Pinschers. Plasma concentrations of other major fatty acids were not significantly different between the 2 breeds. If only the 17 affected dogs were compared, only plasma γ-linolenic acid concentration was significantly (P = 0.03) different between the 13 Boxers and 4 Doberman Pinschers.

For all 51 dogs as a group, there were no significant correlations between plasma fatty acid concentrations and VPC frequency. However, in Boxers, but not in Doberman Pinschers, concentrations of oleic acid (C18:1 n-9; r = 0.37; P = 0.02), total n-9 fatty acids (r = 0.37; P = 0.02), and total n-3 fatty acids (r = 0.37; P = 0.02) were positively, but weakly, correlated with VPC frequency. If only the 17 affected dogs were considered (13 Boxers and 4 Doberman Pinschers), plasma total n-3 fatty acid concentrations were significantly correlated with VPC frequency (r = 0.52; P = 0.03).

Discussion

Results of this study suggested that some plasma fatty acid concentrations were different between the Doberman Pinschers and Boxers, both at the level of certain individual fatty acids (eg, γ-linolenic acid and arachidonic acid) and at the level of specific types of fatty acids (eg, total n-6 fatty acids and total polyunsaturated fatty acids). Although differences in plasma and myocardial fatty acids have been reported for dogs with DCM, compared with healthy controls, breed-specific differences in plasma fatty acid concentrations have not been previously reported.6,7

In addition to plasma fatty acid concentration differences, the relationships between types of fatty acids and VPC frequency may have differed between dogs of the 2 breeds in this study, although further investigation is required. In Boxers, concentrations of total n-3 fatty acids, oleic acid (C18:1 n-9), and total n-9 fatty acids were positively, although not strongly, correlated with VPC frequency, whereas in Doberman Pinschers, there were no significant correlations. When only the 17 affected dogs were included, there was a significant correlation between plasma total n-3 fatty acid concentrations and VPC frequency for both breeds combined. A lack of correlation in the Doberman Pinschers may have been attributable to the small number of dogs of this breed. The weak positive correlations between n-3 fatty acids and arrhythmia reported in the present study differed from results in earlier studies8,10,11,13,14 of experimental animals and humans, in which n-3 fatty acids have been reported to confer protection from ventricular arrhythmia. Notably, in a recent clinical trial limited to Boxers with ARVC, supplementation with EPA and DHA reduced VPC frequency, and n-3 fatty acid concentration was negatively correlated with percentage change in VPC frequency in dogs that received EPA and DHA.11 The negative correlation in that study between n-3 fatty acids and change in VPC frequency detected in dogs that received EPA and DHA suggested to the authors that a minimum threshold concentration of n-3 fatty acids might be required for an effect on VPC frequency to be detected.11 In the present study, median concentrations of total n-3 were substantially lower in Boxers and Doberman Pinschers (3.4% and 3.0%, respectively) than concentrations in dogs that received EPA and DHA in the previous clinical trial in Boxers with ARVC.11 The lack of a negative correlation between n-3 fatty acid concentration and frequency of VPCs in light of the relatively low n-3 fatty acid concentrations in the present study may support the hypothesis that a threshold concentration of n-3 fatty acid is needed to affect frequency of VPCs. Compared with n-3 fatty acids, relationships between n-9 fatty acids and arrhythmias have been much less studied. One study15 evaluating antiarrhythmic effects of various fatty acids in rats not only failed to find an antiarrhythmic effect for oleic acid (C18:1 n-9) but also did not detect a positive correlation.

The reasons for the breed-based differences in plasma fatty acid concentrations in the present study are not clear, but may be related to metabolic differences between Doberman Pinschers and Boxers and differences in the underlying cardiomyopathies. The histologic lesions typically associated with the 2 forms of cardiomyopathy overlap in some respects and differ in others. Although myocyte loss and fibrous replacement occur with both forms of disease, the adipocyte replacement of cardiomyocytes that characterizes Boxers with ARVC has not consistently been documented in Doberman Pinschers with DCM.3,16 Another difference between the cardiomyopathies in the 2 breeds is that, in Boxers, ARVC lesions tend to originate or predominate in the right ventricle, in contrast with the left-sided or biventricular changes that characterize DCM in Doberman Pinschers.2,16,17 The extensive cardiac remodeling associated with DCM may have greater implications for systolic function than does ARVC. In the present study, fractional shortening was reduced to < 25% in 2 of 13 Dobermans Pinschers but in only 1 of 38 Boxers; however, caution in interpretation is necessary because of the small number of dogs with reduced fractional shortening. The metabolic consequences of reduced systolic function in DCM may differ from the right-sided cardiomyopathic lesions of ARVC that may cause a high frequency of arrhythmia without severely impairing cardiac function.

There are several limitations to this study that could have affected outcomes and complicated the interpretation of results. Because detailed diet histories were not available, intakes of n-3 fatty acids were unknown and plasma n-3 fatty acid concentrations were highly variable, especially in the Boxers. In addition, 5 dogs were receiving thyroxine, which at higher doses can increase susceptibility to arrhythmias. It is not known how many of the dogs that were not considered affected by ARVC or DCM will eventually develop cardiomyopathy, and this may complicate the interpretation of fatty acid differences and correlations. Finally, the cutoff value to define dogs as affected with ARVC is controversial in the veterinary cardiology community. In the present study, we chose to use > 100 VPCs/24 h as the cutoff value to consider a dog affected, but further work will be needed to establish whether this value is the most appropriate. Future studies are needed to confirm these results, to determine whether fatty acid metabolism differs in Boxers and Doberman Pinschers, and to evaluate the effect of fatty acid intake on arrhythmia frequency in Doberman Pinschers.

ABBREVIATIONS

DCM

Dilated cardiomyopathy

ARVC

Arrhythmogenic right ventricular cardiomyopathy

CHF

Congestive heart failure

EPA

Eicosapentaenoic acid

DHA

Docosahexaenoic acid

VPC

Ventricular premature complexes

a.

Vingmed Ultrasound, Vingmed-General Electric, Horten, Norway.

b.

Del Mar CardioCorder Recorder Model 459, Del Mar Medical Systems Inc, Irvine, Calif.

c.

AccuPlus model 363 Holter Analysis System, Del Mar Medical Systems Inc, Irvine, Calif.

d.

Lipid Technologies, LLC, Austin, Minn.

e.

AnalTech, Newark, Del.

f.

Supelco, Bellefonte, Pa.

g.

NuCheck Prep, Elysian, Minn.

h.

Model GC17, Shimadzu, Tokyo, Japan.

i.

EZChrom, Scientific Software, Pleasanton, Calif.

j.

Systat, version 10.0, SPSS, Chicago, Ill.

References

  • 1.

    Petric AD, Stabej P, Zemva A. Dilated cardiomyopathy in Doberman Pinschers: survival, causes of death and a pedigree review in a related line. J Vet Cardiol 2002;4:1724.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Calvert CA, Pickus CW, Jacobs GJ, et al. Signalment, survival, and prognostic factors in Doberman Pinschers with end-stage cardiomyopathy. J Vet Intern Med 1997;11:323326.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Basso C, Fox PR, Meurs KM, et al. Arrhythmogenic right ventricular cardiomyopathy causing sudden cardiac death in boxer dogs: a new model of human disease. Circulation 2004;109:11801185.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Meurs KM, Spiers AW, Miller MW, et al. Familial ventricular arrhythmias in Boxers. J Vet Intern Med 1999;13:437439.

  • 5.

    Davila-Roman VG, Vedala G, Herrero P, et al. Altered myocardial fatty acid and glucose metabolism in idiopathic dilated cardiomyopathy. J Am Coll Cardiol 2002;40:271277.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Freeman LM, Rush JE, Kehayias JJ, et al. Nutritional alterations and the effect of fish oil supplementation in dogs with heart failure. J Vet Intern Med 1998;12:440448.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Smith CE, Freeman LM, Meydani M, et al. Myocardial concentrations of fatty acids in dogs with dilated cardiomyopathy. Am J Vet Res 2005;66:14831486.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Billman GE, Kang JX, Leaf A. Prevention of sudden cardiac death by dietary pure omega-3 polyunsaturated fatty acids in dogs. Circulation 1999;99:24522457.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Marchioli R, Barzi F, Bomba E, et al. Early protection against sudden death by n-3 polyunsaturated fatty acids after myocardial infarction: time-course analysis of the results of the Gruppo Italiano per lo Studio della Sopravivenza nell'Infarto Miocardico (GISSI)-Prevenzione. Circulation 2002;105:18971903.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Pepe S, McLennan PL. Dietary fish oil confers direct antiarrhythmic properties on the myocardium of rats. J Nutr 1996;126:3442.

  • 11.

    Smith CE, Freeman LM, Rush JE, et al. Omega-3 fatty acids in Boxer dogs with arrhythmogenic right ventricular cardiomyopathy. J Vet Intern Med 2007;21:265273.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911917.

  • 13.

    GISSI-Prevenzione Investigators. Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Lancet 1999;354:447455.

    • Search Google Scholar
    • Export Citation
  • 14.

    Albert CM, Campos H, Stampfer MJ, et al. Blood levels of longchain n-3 fatty acids and the risk of sudden death. New Engl J Med 2002;346:11131118.

  • 15.

    McLennan PL. Relative effects of dietary saturated, monounsaturated, and polyunsaturated fatty acids on cardiac arrhythmias in rats. Am J Clin Nutr 1993;57:207212.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Calvert CA, Hall G, Jacobs G, et al. Clinical and pathological findings in Doberman Pinschers with occult cardiomyopathy that died suddenly or developed congestive heart failure: 54 cases (1984–1991). J Am Vet Med Assoc 1997;210:505511.

    • Search Google Scholar
    • Export Citation
  • 17.

    Kraus MS, Moise NS, Rishniw M, et al. Morphology of ventricular arrhythmias in the boxer as measured by 12-lead electrocardiography with pace-mapping comparison. J Vet Intern Med 2002;16:153158.

    • Crossref
    • Search Google Scholar
    • Export Citation

Contributor Notes

Dr. Meurs' present address is Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, WA 99164. Supported by the Barkley Fund.

Presented in abstract form at the American College of Veterinary Internal Medicine Forum, Baltimore, June 2005.

Address correspondence to Dr. Freeman.