Association of Plasma Lipid Levels With Atherosclerosis Prevalence in Psittaciformes Author(s): Hugues Beaufrère, Dr Med Vet, PhD, Dipl ABVP (Avian), Dipl ECZM (Avian), Carolyn Cray, PhD, Mélanie Ammersbach, DVM, and Thomas N. Tully Jr, DVM, MS, Dipl ABVP (Avian), Dipl ECZM (Avian) Source: Journal of Avian Medicine and Surgery, 28(3):225-231. Published By: Association of Avian Veterinarians DOI: http://dx.doi.org/10.1647/2013-030 URL: http://www.bioone.org/doi/full/10.1647/2013-030

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Journal of Avian Medicine and Surgery 28(3):225–231, 2014 Ó 2014 by the Association of Avian Veterinarians

Retrospective Study

Association of Plasma Lipid Levels With Atherosclerosis Prevalence in Psittaciformes Hugues Beaufre` re, Dr Med Vet, PhD, Dipl ABVP (Avian), Dipl ECZM (Avian), Carolyn Cray, PhD, Me´ lanie Ammersbach, DVM, and Thomas N. Tully Jr, DVM, MS, Dipl ABVP (Avian), Dipl ECZM (Avian) Abstract: The prevalence of atherosclerosis is high in the captive psittacine population and increases with age and female sex. The genera Psittacus, Amazona, and Nymphicus are predisposed to atherosclerosis, whereas the genera Cacatua and Ara are less susceptible. Plasma cholesterol and lipoprotein abnormalities have been suggested as risk factors in the development of atherosclerosis as observed in mammals. To investigate whether the psittacine genera susceptibility to atherosclerosis and the known risk factors of age and sex could be associated with differences in the lipid profile, a retrospective analysis was conducted on blood lipid values from 5625 birds. Prevalence values were obtained from a previously published, large, case-control study and were compared with identified trends in plasma lipid profiles. Genus-specific differences were identified in plasma total cholesterol values that corresponded to observed trends in the prevalence of clinically important atherosclerotic lesions, which were also highly correlated. The effect of age was significant but was mild and may not account for the dramatic increase in atherosclerosis prevalence observed with age. In addition, Quaker parrots (Myiopsitta monachus), which were used as experimental models for psittacine atherosclerosis and dyslipidemia, were found to have the highest values in all lipid profile parameters. The results of this study suggest that the differences observed in prevalence among species of the psittacine genera may partly be explained by differences in plasma total cholesterol levels. Results also support the use of Quaker parrots as models for studying atherosclerosis and dyslipidemia. Key words: atherosclerosis, cholesterol, triglycerides, lipoproteins, psittacine, Psittaciformes, avian, Quaker parrot, Myiopsitta monachus

with African grey parrots (Psittacus erithacus), Amazon parrots (Amazona species), and cockatiels (Nymphicus hollandicus) appearing to be prone to atherosclerosis, whereas cockatoos (Cacatua species) and macaws (Ara species) were determined to be somewhat resistant to atherosclerosis in a large, multicenter, case-control study that encompassed more than 7600 psittacine birds.1 The reasons for the different predisposition among species in captivity are speculative and could be associated with different captive lifestyles, stress levels, dietary requirements, and/or genetic factors. In the absence of advanced calcification of the atherosclerotic lesions and until significant advances in avian diagnostic imaging are achieved, the diagnosis of atherosclerosis antemortem remains challenging, with diagnosis confirmation usually requiring a postmortem examination of the car-

Introduction Atherosclerosis is a common lesion on postmortem examination in Psittaciformes, and the prevalence of clinically important atherosclerotic lesions, significant enough to induce clinical signs, is high in psittacine birds and increases with age and female sex.1–11 Differences in genera susceptibility to atherosclerosis have also been observed, From the Health Sciences Centre (Beaufr`ere) and the Department of Pathobiology (Ammersbach), Ontario Veterinary College, University of Guelph, 50 Stone Rd, Guelph, ON N1G 2W1, Canada; the Division of Comparative Pathology, Department of Pathology, Miller School of Medicine, University of Miami, 1600 NW 10th Ave, Miami, FL 33136, USA (Cray), and the Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Skip Bertman Dr, Baton Rouge, LA 70803, USA (Tully).

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diovascular system. Therefore, risk factors that may partially explain the observed variability in atherosclerosis susceptibility among species, particularly biochemical markers, remains challenging to study in psittacine species. High total blood cholesterol levels, increased low-density lipoprotein (LDL) levels, and decreased high-density lipoprotein (HDL) levels are considered major risk factors for atherosclerosis in humans and are the principal targets for preventative therapies.12–14 This is due to the central role of lipids in the pathogenesis of atherosclerosis.15–18 Total and LDL cholesterol concentrations increase with age in humans and partially explain the agerelated increase in coronary heart disease.19–21 Likewise, these parameters increase with age in some laboratory animals, such as rats (Rattus norvegicus).22 However, the distribution of cholesterol with age, species, and sex is not known in psittacine birds, and similar trends may be present. Dyslipidemic changes with hypercholesterolemia are thought to predispose psittacine birds, as in other animal species, to the development of atherosclerotic lesions. African grey and Amazon parrots, which have a higher prevalence of atherosclerosis, tend to have higher plasma cholesterol levels than do other psittacine species, but the magnitude of those differences and their association with prevalence differences of this disease have not, to our knowledge, been investigated.1,23 Total plasma cholesterol has been shown to correlate with the occurrence of atherosclerosis in psittacine birds, but changes in lipoproteins have not yet been explored.11 In a case-control study11 on 22 birds, parrots with atherosclerotic lesions had a significantly higher median (interquartile range) plasma cholesterol at 421 (233–906) mg/dL than did control birds at 223 (144–250) mg/dL, based on their medical records. Atherosclerosis and hypercholesterolemia have been induced in budgerigars (Melopsittacus undulatus) with 2% dietary cholesterol.24,25 Another diet-induced atherosclerosis experiment in Quaker parrots (Myiopsitta monachus) fed a 1% cholesterol diet demonstrated a fivefold and 15-fold increase in plasma total and LDL cholesterol, respectively. In addition, lesion severity and arterial cholesterol content were both significantly correlated to plasma total and LDL cholesterol concentrations.26 Large laboratory data sets are available and, if combined with previous scientific data about the prevalence and risk factors of atherosclerosis, may help identify trends and associations between hematologic data and the lesions. If increased

plasma total and LDL cholesterol are significant risk factors for atherosclerosis in psittacine birds, like they are for other species, we could reasonably argue that genus-, sex-, and age-related trends in these parameters could be detected in psittacine birds and would mirror prevalence trends also observed for these risk factors. With this study, we attempted to identify potential genus-, sex-, and age-related trends in plasma lipid profiles with 2 large, existing data sets of unselected animals. We hypothesized that plasma total and LDL cholesterol concentrations would be greater in females, in some genera, and with increasing age. Materials and Methods Databases Two large clinical pathology databases were used in this study from the Avian and Wildlife Laboratory, Division of Comparative Pathology, Department of Pathology, Miller School of Medicine, University of Miami, Miami, FL, USA (3713 birds, from 2005 to 2012) and the Animal Health Laboratory, Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada (1912 birds, from 1998 to 2012). Information was extracted from the databases for 6 genera (Myiopsitta [Quaker parrots], Psittacus [African grey parrots], Amazona [Amazon parrots], Nymphicus [cockatiels], Cacatua [cockatoos], and Ara [macaws]) for plasma cholesterol levels, lipoprotein (HDL, LDL) levels, sex, and age. Cholesterol analysis was performed on 5625 birds. Lipoprotein (HDL, LDL) analysis was only performed on 379 birds (6.7%) and at only one of the two centers. Triglycerides analysis was performed on 1914 birds (34.0%). Cholesterol, triglycerides, and HDL were directly measured values, but LDL was calculated with the Friedewald formula.27 Analytes were measured with an Ortho Vitros Chemistry System at the University of Miami (Ortho-Clinical Diagnostics Inc, Rochester, NY, USA) and with a Roche Cobas c501 (F. Hoffmann-La Roche Ltd, Basel, Switzerland) and a Hitachi 911 (Hitachi Ltd, Chiyoda, Tokyo, Japan) at the University of Guelph; extensive cross-validations between the 2 analyzers were performed as part of standard diagnostic laboratory procedures. Because of financial constraints and the retrospective nature of the study, cross-validation between the 2 veterinary laboratories was not performed. However, all machines used the same biochemical reactions to measure cholesterol and triglyceride levels. For cholesterol, the assay consisted of an

´ BEAUFRERE ET AL—PLASMA LIPIDS AND ATHEROSCLEROSIS IN PSITTACIFORMES

enzymatic, calorimetric method whereby cholesterol esters were cleaved by the action of cholesterol esterase to yield free fatty acids and cholesterol. Cholesterol oxidase then catalyzed the oxidation of cholesterol, during which, hydrogen peroxide was generated. Hydrogen peroxide affects the oxidative coupling of phenol and 4aminophenazone to form a red quinone-imine dye that is measured by increasing absorbance. For triglycerides, the assay consisted of an enzymatic reaction whereby triglyceride esters were cleaved into glycerol and free fatty acids. Glycerol was then phosphorylated into glycerol-3-phophate and oxidized in dihydroxyacetone phosphate and hydrogen peroxide. Hydrogen peroxide was detected by the same reaction as previously described. Information on age and sex were only available for 20% of the data set (1125/5625 birds). Because clinical information was most often not available for laboratory blood submissions, no other inclusion criteria, other than availability of cholesterol values, were used in this study. Fasting for 6–12 hours is recommended for submission of avian samples; however, because of the retrospective nature of this study, that could not be verified. Only the 6 psittacine genera were used because detailed prevalence information is available in 5 of them (Psittacus, Amazona, Nymphicus, Cacatua, Ara) and the genus Myiopsitta has been used as an experimental model for atherosclerosis and dyslipidemia.1,26,28,29 Statistical analysis The association among the outcome variables (cholesterol, triglycerides, LDL, and HDL) and the independent variables (age, sex, species, interaction terms) could not be assessed by multiple linear regression because of the nonnormality of the residuals. Transformations of the data, including log, square root, and rank, were unsuccessful in achieving normality of residuals. Therefore, associations were investigated with distribution-free, univariate tests. In addition, because cross-validation of the assays between the 2 centers was not performed, descriptive statistics on the population used were performed with graphical methods (mosaic and violin plots) to determine whether a bias in data distribution was visually obvious. Species and center differences in plasma cholesterol levels were investigated with the complete database, whereas age and sex associations with plasma cholesterol levels were assessed only with the 20% of the data set (1125 birds) that included such

227

information. Species differences in median were assessed with a Kruskal-Wallis analysis of variance, sex and center differences with Wilcoxon rank-sum tests, and age association with Spearman correlation coefficient. Nonparametric multiple comparisons were performed on species with a Tukey adjustment. The association between the median cholesterol values and the prevalence of atherosclerosis for the different genera was evaluated as follows: The prevalence of atherosclerosis as a function of age was known in all genera investigated, except Myiopsitta, from a large epidemiological study1 previously performed on more than 7600 individuals. The prevalence is a sigmoid function (logistic) of the age. From previously determined prevalence logistic functions,1 the area under the curve (AUC) was obtained for all genera by integrating the logistic functions between 0 and 30 years. Thirty years corresponded to the 95% percentile of the age of the population in the data set used in the present study. Then, the association between the cholesterol median values and the prevalence AUC was assessed with a Pearson correlation coefficient, except for Myiopsitta. R software (R Foundation for Statistical Computing, Vienna, Austria) was used for statistical analysis and computation of integrals. Results The demographics of the population studied were similar between the 2 centers, and the distribution of genera was also homogeneous between the 2 centers, except for Quaker parrots. The relative frequency of males and females was also comparable within centers and psittacine genera. The distribution of total cholesterol within centers and psittacine genera was also comparable between centers. There was a significant difference between species in the median plasma cholesterol, triglycerides, LDL, and HDL (Kruskal-Wallis, P , .001). Quaker parrots had a significantly higher median cholesterol value than did other species. Amazon parrots, African grey parrots, and cockatiels had similar cholesterol levels but were lower than Quaker parrots and higher than cockatoos and macaws (Table 1). Cockatoos had significantly higher cholesterol levels than macaws did. The pattern in triglyceride differences was similar to that of cholesterol, except for Psittacus, which was in the lowest triglyceride level group but in the high cholesterol group. Quaker parrots had significantly higher and macaws had significantly lower median LDL levels than other species. For HDL, only

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Table 1. Cholesterol panel values in 6 psittacine genera. Psittacine generaa Cholesterol panel

Cholesterol, mg/dL

Triglycerides, mg/dL

LDL, mg/dL

HDL, mg/dL

Myiopsitta

N Median P25 P75 N Median P25 P75 N Median P25 P75 N Median P25 P75

247 344.0 276.0 475.5 143 319.0 200.0 448.0 70 207.0 72.5 303.7 70 128.0 109.2 185.0 NA

AUC (0–30)

A

A

A

A

Amazona

Psittacus

1427 248.0 200.0 323.0 506 172.5 123.2 297.5 166 99.2 48.2 170.9 166 122.0 110.0 134.5 72.3

1254 246.9 213.1 288.0 338 117.0 95.0 149.8 38 96.8 51.0 165.0 38 126.5 112.2 140.5 81.6

B

C

B

A

B

D

B

A

Nymphicus

447 246.9 195.5 337.8 169 223.0 139.0 318.0 34 108.5 33.1 246.0 34 122.5 109.2 134.5 66.8

B

B

B

A

Cacatua

1064 207.0 176.0 252.0 298 107.5 78.0 156.0 34 105.4 29.2 179.7 34 113.5 98.5 123.2 23.1

C

D

B

A

Ara

1186 159.7 134.0 193.3 460 110.0 83.0 164.5 37 32.0 12.2 89.0 37 109.0 87.0 125.0 13.9

D

D

C

B

Abbreviations: N indicates the number of birds; P25, 25th percentile; P75, 75th percentile; LDL, low-density lipoprotein cholesterol; HDL, high-density lipoprotein cholesterol; AUC, area under the atherosclerosis prevalence curve between 0 and 30 years; NA, not applicable. a

Within each row, values with small capital significantly different.

A

were significantly greater than B,

macaws showed a significantly lower median HDL level than other species (Table 1). There was a weak but significant correlation of age with cholesterol and triglyceride levels (q ¼ 0.06, P , .001, and q ¼ 0.19, P , .001, respectively) and no significant correlation with LDL and HDL. There was no significant effect of sex on the plasma cholesterol levels (Wilcoxon, P ¼ .35), triglyceride levels (Wilcoxon, P ¼ 0.10), LDL (Wilcoxon, P ¼ .70), and HDL levels (Wilcoxon, P ¼ .09). There was no significant difference between centers on any of the values, and no trend was observed. The Pearson correlation coefficients between the cholesterol, triglyceride, LDL, and HDL median levels and the atherosclerosis prevalence AUC (obtained from a previous study) was 0.93 (P ¼ .02), 0.53 (P ¼ .36), 0.62 (P ¼ .27), and 0.99 (P ¼ .002), respectively (Fig 1). When the data set was trimmed for the 5% highest values, which might skew the data set from highly dyslipidemic animals, the observed trends were similar, indicating that those extreme values did not have a strong effect on the results. Discussion In this study, we identified genus-specific differences in plasma total cholesterol values that mirror observed trends in the prevalence of clinically

B

. C,

C

. D. Values with the same superscript were not

important atherosclerotic lesions in avian genera, except in Quaker parrots, for which that prevalence information was not available. In the genera in this study, age was significantly associated with cholesterol and triglyceride levels, but the association was weak. Cholesterol, triglyceride, HDL, and LDL levels did not differ significantly between sexes, which invalidated that part of our hypothesis. The genus Ara, the least susceptible genus to atherosclerosis, was found to have the lowest LDL and HDL median values. Quaker parrots were found to have significantly higher values than any other genus in all lipid profile parameters, but the sample size was much smaller than it was for other species included in this study. A high correlation with atherosclerosis prevalence was found with increasing HDL but not LDL. The results of this study suggest that the differences observed in prevalence among psittacine genera may be explained in part by differences in plasma total cholesterol levels. All species were fed roughly a similar diet in captivity, but it is known that some species consume a diet with higher fat content in the wild, such as macaws.30 Consequently, differences observed among genera in plasma cholesterol levels and atherosclerosis prevalence are possibly associated with different fat nutritional requirements and the lipid metabolism abilities of different species, with atherosclerosis-resistant species being better ‘‘equipped’’ to

´ BEAUFRERE ET AL—PLASMA LIPIDS AND ATHEROSCLEROSIS IN PSITTACIFORMES

229

Figure 1. Scatterplot of the median cholesterol (left) and high-density lipoprotein (HDL) (right) values (mg/dL) against the atherosclerosis prevalence for area under the curve (AUC) values obtained from a previous study1 (Pearson correlation coefficient, 0.93 and 0.99, respectively). Each dot represents one genus.

metabolize lipids. In captivity, parrots are given the same diet year-round, with little variability and consideration for physiologic status and season. In addition, some species may be more active and may not adapt metabolically as well as other species to the sedentary nature and the ad libitum provision of high-energy food in captivity. However, only an association was observed here, and the presence of confounding factors or other factors that concurrently raise both plasma cholesterol and atherosclerosis prevalence are possible. Interestingly, Quaker parrots had the highest cholesterol, triglyceride, and lipoprotein levels of the genera in this study. The difference was large, with a 55% increase in median cholesterol level and 134% increase in median LDL levels compared with other psittacine genera. Quaker parrots are good models for experimental atherosclerosis because they develop advanced lesions quickly and display extreme dyslipidemia, but our findings reinforce the rationales behind using Quaker parrots as a model for psittacine atherosclerosis investigations. Triglyceride levels followed the same trend as total cholesterol levels, except for African grey parrots, which had lower values than expected. A higher correlation with age was found with triglycerides levels than with cholesterol levels. However, no significant correlation was found with recorded prevalence in the genera investigated. Hypertriglyceridemia is a prominent risk factor for atherosclerosis in humans because triglycerides contain atherogenic lipoproteins, such as very low-density lipoprotein.31 Cockatiels had significantly higher triglycerides values than did other genera, except Myiopsitta. This finding may be associated with the high prevalence of reproductive disorders in this species. Postprandial effects on triglycerides levels are dramatic, but because of the

retrospective nature of this study, we cannot ascertain that plasma samples were obtained from fasted birds. Some lipoprotein findings were unexpected in this study. The LDL median values did not correlate with increasing atherosclerosis prevalence AUC, and the genus Ara, which is atherosclerosisresistant, had the lowest LDL and HDL values. The strong correlation between HDL and atherosclerosis prevalence AUC is difficult to explain. Therefore, higher HDL values may not be associated with decreased risks of developing atherosclerosis in psittacine birds like it is in mammals. Similar to most birds, psittacine birds transport cholesterol mainly in the form of HDL, whereas LDL is the preponderant form in humans. Differences in avian lipoprotein metabolism may have some implications in the pathogenesis of psittacine atherosclerosis.26,32 Unknown factors may have also confounded the study results. Additionally, the sample size for lipoprotein data was much smaller than it was for total cholesterol analysis and was unbalanced among the genera (see Table 1 for sample sizes). In addition, in a nutritional atherosclerosis induction study,26 HDL levels did not increase with cholesterol feeding in Quaker parrots. However, it is difficult to conceive that the very high linear correlations (0.93–0.99, see Fig 1) observed would be entirely due to chance and the presence of distribution biases. Finally, the validity of HDL laboratory measurement methods and the use of the Friedewald formula to estimate the LDL have not been thoroughly investigated in birds, despite encouraging preliminary results.33 The dramatic increase in atherosclerosis prevalence previously observed with age may not be associated with a corresponding age-related increase in plasma cholesterol and triglycerides levels but may be better explained by other risk factors

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and age-related mechanisms.1 Likewise, female sex was not associated with increased plasma cholesterol levels, despite a much larger prevalence observed in female psittacine birds than in males and drastic blood lipid changes brought about by the female birds’ reproductive cycle.1 Increases in cholesterol and triglyceride levels may be short lived in female birds, and blood samples used in this study represent a single point in time. Serial blood cholesterol values would likely be more valuable in exploring the association between atherosclerotic risks and female-specific lipid metabolism. Also, sex determination was based on submission forms, and a subset of our data may not have been accurate because the method of sex determination was not available. The results of this study should be interpreted in light of its many limitations. We retrospectively used data sets with unselected birds that likely contained both healthy and unhealthy animals. Some genera may also be predisposed to other diseases that can elevate cholesterol levels, such as endocrine, reproductive, and metabolic diseases. However, valuable clinical pathologic information can still be derived from a large data set with unselected animals and undefined inclusion criteria when clinical information is not available in sufficient amount or detail to determine health status.34 Also trimming the upper 5% of lipid profile values did not alter our results. Another limitation of this study was the inability to use multivariable statistics because of the extreme skewness of the data distribution. Multivariable statistics would have allowed more robust analysis with finer interpretation of the results controlling for potential confounding variables, such as age and sex. As such, our analysis was not controlled for confounding variables, and findings may be different in subsequent studies when more clinical information is present and multivariable analysis is performed. Retrospective data sets may be hard to work with, and although our indiscriminate approach had some limitations, it was still useful for identifying potential effects and hypotheses to be confirmed with future prospective studies that consume more time and resources. This approach allowed us to explore possible associations with a large sample size on a representative population of birds. Some birds may have been represented in this study as repeated measures, but although some blood values may be correlated within birds, we do not expect that to significantly affect the statistical results in a large data set such as the one used in this investigation. Finally, it should be emphasized

that nothing can be concluded on the clinical value of plasma lipid profile at the individual level because our goal was to investigate populationwide associations. The value of lipid profile screening to identify individual psittacine patients at increased risks of developing atherosclerotic diseases should be investigated with retrospective and prospective studies with more complete clinical and pathologic information. References 1. Beaufr`ere H, Ammersbach M, Reavill D, et al. Prevalence of and risk factors associated with atherosclerosis in psittacine birds. J Am Vet Med Assoc. 2013;242(12):1696–1704. 2. Bavelaar FJ, Beynen AC. Severity of atherosclerosis in parrots in relation to the intake of alpha-linolenic acid. Avian Dis. 2003;47(3):566–577. 3. Fricke C, Schmidt V, Cramer K, et al. Characterization of atherosclerosis by histochemical and immunohistochemical methods in African grey parrots (Psittacus erithacus) and Amazon parrots (Amazona spp.). Avian Dis. 2009;53(3):466–472. 4. Garner MM, Raymond JT. A retrospective study of atherosclerosis in birds. Proc Annu Conf Assoc Avian Vet. 2003:59–66. 5. Kellin N. Auswertung der Sektions- und Laborbefunde von 1780 V¨ogeln der Ordnung Psittaciformes in einem Zeitraum von vier Jahren (2000 bis 2003) [doctoral thesis]. Giessen, Germany: University of Giessen. 2009:252. 6. Krautwald-Junghanns M, Braun S, Pees M, et al. Research on the anatomy and pathology of the psittacine heart. J Avian Med Surg. 2004;18(1):2–11. 7. Johnson JH, Phalen DN, Kondik VH, et al. Atherosclerosis in psittacine birds. Proc Annu Conf Assoc Avian Vet. 1992:87–93. 8. Beaufr`ere H, Nevarez JG, Holder K, et al. Characterization and classification of psittacine atherosclerotic lesions by histopathology, digital image analysis, transmission and scanning electron microscopy. Avian Pathol. 2011;40(5):531–544. 9. Dorrestein GM, Zwart P, Borst GHA, et al. Causes of disease and death in birds [in Dutch]. Tijdschr. Diergeneeskd. 1977;102(7):437–447. 10. Finlayson R. Spontaneous arterial disease in exotic animals. J Zool. 1965;147:239–343. 11. Pilny AA, Quesenberry KE, Bartick-Sedrish TE, et al. Evaluation of Chlamydophila psittaci infection and other risk factors for atherosclerosis in pet p s i t t a c i n e bi r d s . J A m V et Me d A s s oc . 2012;240(12):1474–1480. 12. von Eckardstein A. Risk factors for atherosclerotic vascular disease. In: von Eckardstein A, ed. Atherosclerosis: Diet and Drugs. Handbook of Experimental Pharmacology. Vol 170. Berlin, Germany: Springer; 2005:71–105.

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13. Pearson TA, Blair SN, Daniels SR, et al. AHA guidelines for primary prevention of cardiovascular disease and stroke: 2002 update: consensus panel guide to comprehensive risk reduction for adult patients without coronary or other atherosclerotic vascular diseases. Circulation. 2002;106(3):388–391. 14. Kavey RE, Daniels SR, Lauer RM, et al; American Heart Association. American Heart Association guidelines for primary prevention of atherosclerotic cardiovascular disease beginning in Childhood. Circulation. 2003;107(11):1562–1566. 15. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature. 2011;473(7347):317–325. 16. Falk E. Pathogenesis of atherosclerosis. J Am Coll Cardiol. 2006;47(suppl 8):C7–C13. 17. Cullen P, Rauterberg J, Lorkowski S. The pathogenesis of atherosclerosis. In: von Eckardstein A, ed. Atherosclerosis: Diet and Drugs. Handbook of Experimental Pharmacology. Vol 170. Berlin, Germany: Springer; 2005:3–70. 18. George SJ, Lyon C. Pathogenesis of atherosclerosis. In: George SJ, Johnson J, eds. Atherosclerosis: Molecular and Cellular Mechanisms. Weinhein, Germany: Wiley-VCH Gmbh & Co; 2010:3–20. 19. Abbott RD, Garrison RJ, Wilson PW, et al. Joint distribution of lipoprotein cholesterol classes: the Framingham study. Arteriosclerosis. 1983;3(3):260– 272. 20. Jousilahti P, Vartiainen E, Tuomilehto J, Puska P. Sex, age, cardiovascular risk factors, and coronary heart disease: a prospective follow-up study of 14 786 middle-aged men and women in Finland. Circulation. 1999;99(9):1165–1172. 21. Gostynski M, Gutzwiller F, Kuulasmaa K, et al; WHO MONICA Project. Analysis of the relationship between total cholesterol, age, body mass index among males and females in the WHO MONICA Project. Int J Obes Relat Metab Disord. 2004;28(8):1082–1090. 22. Uchida K, Nomura Y, Kadowaki M, et al. Agerelated changes in cholesterol and bile acid metabolism in rats. J Lipid Res. 1978;19(5):544–552.

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23. Bavelaar FJ, Beynen AC. Atherosclerosis in parrots: a review. Vet Q. 2004;26(2):50–60. 24. Finlayson R, Hirchinson V. Experimental atheroma in budgerigars. Nature. 1961;192(4800):369–370. 25. Petzinger C, Heatley JJ, Cornejo J, et al. Dietary modification of omega-3 fatty acids for birds with atherosclerosis. J Am Vet Med Assoc. 2010;236(5):523–528. 26. Beaufr`ere H, Nevarez JG, Wakamatsu N, et al. Diet-induced experimental atherosclerosis in Quaker parrots (Myiopsitta monachus). Vet Pathol. 2013;50(6):1116–1126. 27. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18(6):499–502. 28. Petzinger C, Larner C, Heatley J, Bauer J. HDL density subfraction alterations and plasma lipids with dietary polyunsaturated fatty acids in Myiopsitta monachus. Proc Annu Conf Assoc Avian Vet. 2011:297–298. 29. Petzinger C. Lipid Metabolism, Learning Ability and Potential Biomarkers for Atherosclerosis in Monk Parrots (Myiopsitta monachus) Fed n-3 Fatty Acids [PhD dissertation]. College Station, TX: Texas A&M University. 2012:1–159. 30. Brightsmith DJ, McDonald D, Matsafuji D, Bailey CA. Nutritional content of the diets of free-living scarlet macaw chicks in southeastern Peru. J Avian Med Surg. 2010;24(1):9–23. 31. Talayero BG, Sacks FM. The role of triglycerides in atherosclerosis. Curr Cardiol Rep. 2011;13(6):544– 552. 32. Xiangdong L, Yuanwu L, Hua Z, et al. Animal models for the atherosclerosis research: a review. Protein Cell. 2011;2(3):189–201. 33. Cray C. Analysis of psittacine lipoproteins. Proc Annu Conf Assoc Avian Vet. 2007:257–259. 34. Dimauro C, Bonelli P, Nicolussi P, et al. Estimating clinical chemistry reference values based on an existing data set of unselected animals. Vet J. 2008;178(2):278–281.

Association of plasma lipid levels with atherosclerosis prevalence in psittaciformes.

The prevalence of atherosclerosis is high in the captive psittacine population and increases with age and female sex. The genera Psittacus, Amazona, a...
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