A four-week white bread diet does not alter plasma glucose concentrations, metabolic or vascular physiology in mourning doves, Zenaida macroura

https://doi.org/10.1016/j.cbpa.2020.110718Get rights and content

Highlights

  • Mourning doves fed a four-week white bread diet had minimal changes in metabolite concentrations or metabolic pathways.

  • Plasma glucose concentrations were not altered by a four-week white bread diet.

  • Liver glycogen concentrations were significantly increased following the four-week refined carbohydrate diet.

  • Endothelium-dependent vasodilation of ex vivo cranial tibial arteries was not altered by the white bread diet.

  • In summary, doves maintain metabolic, physiological, and vascular homeostasis in response to a refined carbohydrate diet.

Abstract

Birds are an enigma: their plasma glucose concentration is 1.5–2 times higher than similar-sized mammals, yet they do not normally exhibit symptoms of diabetes. We hypothesized that feeding adult mourning doves a refined carbohydrate diet (white bread: WB) for four weeks would raise plasma glucose concentrations and alter metabolic pathways and endothelial function when compared to birds receiving a nutritionally-balanced diet (bird seeds: SD). Following the four-week long diets, birds were euthanized, and cardiac blood, liver, and pectoralis muscles were collected for metabolomics analyses and biochemical assays. Cranial tibial arteries were dissected to measure acetylcholine-mediated vasodilation. Contrary to the hypothesis, WB-fed birds did not have increased plasma glucose concentrations. Principle component analysis score plots suggest minimal differences between groups. However, we identified 15 changes in individual metabolite concentrations between diet groups that, although not statistically significant, are highly predictive (area under receive operating curve, AUROC>0.90; number of highly predictive metabolites: 5 of 123 in plasma, 4 of 92 in liver, and 6 of 92 in pectoralis muscle). Moreover, pathway analyses revealed no significantly altered metabolic pathways between groups. Biochemical assays revealed no significant group differences in plasma uric acid and insulin, or pectoralis muscle glycogen concentrations. However, hepatic glycogen concentration was 2.12-fold higher in the WB group than in control doves (p = .015). Diet type did not influence vasodilation. In conclusion, a four-week long white bread diet increased liver glycogen but did not alter plasma glucose concentrations, metabolic or vascular physiology in mourning doves.

Introduction

Plasma glucose concentrations are 1.5–2 times higher in birds than in mammals of similar body mass (Braun and Sweazea, 2008). The evolutionary and physiological reasons for this difference are unknown and may include lower plasma insulin in birds than mammals (Hazelwood, 1973), insensitivity to the glucose lowering effects of insulin in birds (Dupont et al., 2004; Sweazea and Braun, 2005; Sweazea et al., 2006), and a higher sensitivity of birds than mammals to the effects of glucagon (Hazelwood, 1973). In fact, only supraphysiological doses of insulin have been shown to moderately lower blood glucose (Chen et al., 1945; Chida et al., 2000; Tokushima et al., 2005). Avian physiology also differs from that of mammals in that lipogenesis in birds predominantly occurs in the liver instead of adipose (Leveille et al., 1968) and absorbed dietary fat enters directly into the bloodstream in the form of portomicrons, instead of circulating through the lymphatic system as seen in mammals (Bensadoun and Rothfeld, 1972). Aside from their unique physiology, birds may serve as a natural model of hyperglycemia without the complications that mammals normally develop, and thus can aide in diabetes research (Szwergold and Miller, 2014).

In rodents, a diet rich in refined carbohydrates can cause adipose tissue inflammation and metabolic derangement (de Oliveira et al., 2013). This diet increases hepatic fat, triglycerides, and total cholesterol (de Oliveira and Menezes-Garcia, 2015), as well as visceral fat and plasma triglycerides (Spadaro et al., 2015), total serum cholesterol, and blood pressure while decreasing insulin sensitivity (Yamada et al., 2016; Fournier et al., 1986). Whether birds, which are naturally hyperglycemic, develop similar pathologies in response to an exclusive refined carbohydrate diet has not been determined. We investigated this question by measuring the effects of a diet consisting of highly refined carbohydrates (commercial white bread) fed to mourning doves. Mourning doves are mostly granivorous (Dillon, 1961) and their natural diet, therefore, consists primarily of complex carbohydrates. However, the processing of whole wheat seeds into white bread makes the stored starch more readily accessible to digestive enzymes and raises the glycemic load (GL) for humans per gram of food from 0.6 to 2.36 GL, thus increasing the rate at which the food is digested and absorbed after eating (Atkinson et al., 2008). Further, as birds predominately absorb monosaccharides via paracellular processes (Caviedes-Vidal et al., 2007), the added simple sugars to bread plus the readily available starch make a bread diet a strong choice to examine physiological responses to a high glycemic diet in birds.

In mammals, chronic hyperglycemia is associated with increased production of reactive oxygen species (ROS; Inoguchi et al., 2000). ROS can contribute to vascular damage such as impaired endothelium-dependent vasodilation, which can promote hypertension (Taniyama and Griendling, 2003). By contrast, mourning doves, although having high plasma glucose, have ROS concentrations that are similar to those of healthy rats (Smith et al., 2011). Studies of cranial tibial arteries from mourning doves found that ex vivo exposure to high glucose concentrations impairs endothelium-mediated vasodilation via an oxidative stress-dependent mechanism (Jarrett et al., 2016). The mechanism that protects intact birds from elevated plasma glucose-associated oxidative damage remains speculative.

Granivorous urban birds often consume human foods typical of a western diet that are obtained from waste or recreational feeding, and bread is reportedly the most common food given to birds by bird feeders (Galbraith et al., 2014). Although wheat seed is a choice food for mourning doves (Hayslette and Mirarchi, 2001), it is unknown how a fully refined wheat/bread diet would affect the metabolic and vascular physiology of these birds. We hypothesized that feeding adult mourning doves a refined carbohydrate diet for four weeks would 1) raise plasma glucose concentrations and alter metabolic pathways related to energy metabolism, and 2) impair vascular function when compared to birds fed nutritionally balanced bird seeds (seed diet). Determining how mourning doves respond to a highly refined carbohydrate diet may help us better understand their unique physiology and identify how granivorous birds in general protect themselves from diet-induced hyperglycemia and resultant diabetes-like pathologies as seen in mammals.

Section snippets

Animals and diet

Mourning doves commonly reside in the study area (Arizona State University [ASU] Tempe Campus; 33° 25′11.5”N - 111° 55′ 55.6”W; altitude: 365 m asl) and have been used for related studies (Jarrett et al., 2016, Jarrett et al., 2013; Smith et al., 2011; Sweazea et al., 2006). Adult male mourning doves (Zenaida macroura; 110–130 g body mass) were trapped as previously described (Jarrett et al., 2016; Jarrett et al., 2013; Smith et al., 2011), using a walk-in funnel trap baited with wild bird

Results

In total, 123 plasma metabolites as well as 92 liver and pectoral muscle metabolites were reliably detected in more than 80% of all samples (Supplemental file). In total, 15 metabolites were notably altered (ROAUC>0.90) although t-test significance was lost for all metabolites after adjusting for multiple hypothesis testing (q-value>0.05; Table 2). Table 2 contains significance information, area under receiver operating characteristic (AUROC) results, as well as fold change (FC) magnitude

Discussion

We used mourning doves as an experimental model to determine the metabolic and physiological effects of consuming a refined carbohydrate diet compared to their natural complex carbohydrate diet. Contrary to our hypothesis, which was based on mammalian response to a refined carbohydrate diet, WB consumption did not alter plasma glucose concentrations in doves, and PCA score plots suggest minimal differences in plasma, liver, and pectoralis muscle metabolites between groups. However, consumption

Acknowledgments

The authors would like to acknowledge Xinchen Wang from the Arizona State University Metabolomic Laboratory for their assistance with the multivariant analyses. We also thank Monique Bertin for her technical assistance with tissue and plasma assays.

Author contributions

KLS, PD and HG were senior authors on the study. AJB, WC, and KLS carried out the plasma and tissue biochemical assays and data analyses. KLS carried out the vasodilation measurements and analyses. AJB, KLS, PD, and HG conceived and planned, while XS, PJ, and HG carried out, the plasma and tissue metabolomics data collection and analyses. AJB, KLS, and PD contributed to the interpretation of the results. AJB took the lead in writing the manuscript and all authors provided critical feedback.

Funding

ASU School of Life Sciences/Office of Knowledge Enterprise Development - Research Investment Initiative (KLS, PD), a summer research fellowship from the American Physiological Society (WC), and an ASU Center of Evolution and Medicine Graduate Fellow Award (AJB).

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper

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