Intake of Watermelon or Its Byproducts Alters Glucose Metabolism, the Microbiome, and Hepatic Proinflammatory Metabolites in High-FatFed Male C57BL/6 J Mice

Abstract

Background Watermelon intake has demonstrated effects on blood pressure regulation along with other health benefits. Objective We hypothesized that intake of whole watermelon and products made from watermelon rind (WR) and watermelon skin (WS) would remediate metabolic complications in C57BL/6 J male mice fed a diet modeling a Western-style diet. Methods Ten-week-old male C57BL/6 J mice were provided either a low-fat (LF) diet [10% fat (by energy), 8% sucrose (by energy) and no added cholesterol], a high-fat (HF) diet [45% fat (by energy), 20% kcal sucrose (by energy), and 1% (w/w) cholesterol], or an HF diet plus WS, WR, or watermelon flesh (WF) for 10 wk. Dried WF was provided at 8% of total energy (equivalent to 2 servings/d) and watermelon skin and rind were added at 2.25% (w/w, dry weight of additives) of diet. Animals were provided experimental diets ad libitum. Body weights, food intake, and glucose tolerance were determined. Serum insulin, inflammatory markers, microbiome, and the relative hepatic concentrations of 709 biochemicals were measured postmortem. Results The final body weight of the LF control group was significantly lower than that of the HF-fed control group (32.8 ± 0.9 g compared with 43.0 ± 1.7 g, P ≤ 0.05). Mice in treatment groups fed HF supplemented with watermelon products had final body weights similar to those of the HF-fed control mice. Serum insulin concentrations were reduced by ∼40% in mice fed an HF diet with WR supplementation compared with mice fed an HF diet alone (P ≤ 0.05). Depending on the individual species or group, microbiome populations changed significantly. Supplementation with WF resulted in a return to the basal hepatic concentrations of monohydroxy fatty acids and eicosanoids observed in LF-fed mice (P ≤ 0.05). Conclusions In obese male mice, supplementation with each of the watermelon products to an HF diet improved fasting blood glucose, circulating serum insulin concentrations, and changes in hepatic metabolite accumulation. At a modest level of supplementation to an HF diet, fiber-rich additives made from WR and WS further improved glucose metabolism and energy efficiency and shifted the microbiome composition.

Intake of Watermelon and Watermelon Byproducts in Male Mice Fed a Western-Style Obesogenic Diet Alters Hepatic Gene Expression Patterns, as Determined by RNA Sequencing

“…Further, cecal bacteria populations from WS-fed mice shifted toward those of LF-fed mice. Thus, when compared to mice in the HF control group, obese mice in each of the WS, WF, and WR groups showed improved fasting blood glucose levels, circulating serum insulin concentrations, and/or changes in hepatic metabolite accumulation ( 19 ).…”

“…lanatus cv. Fascination) grown in Hermiston, Oregon, was prepared as described by Becraft et al ( 19 ). Briefly, the skin was peeled from the outer surface using a common kitchen peeler, and the flesh and rind were sliced into 2”x2”x1/8” sections.…”

“…The dried fruit was powdered and incorporated into the experimental diets. The WF, WR, and WS contained 10.6, 6.6, and 9.6% moisture, respectively; 89.4, 93.4, and 90.4% solids, respectively; and 4, 46.2, and 64.5% of dietary fiber, respectively ( 19 ).…”

“…There were 3 treatment groups, which were each fed a HF diet supplemented with either dried WF at 8% total energy (kcal), WR at 2.25% (w/w), or WS at 2.25% (w/w; Supplemental Table 1 ). We balanced the macronutrients such that every HF-based diet contained the same total percentage of each macronutrient, but with different fiber and phytochemical contents depending on the foods added, as previously described by Becraft et al ( 19 ). The WF was included in the diets at 8% of total energy, to model the human intake of 2 servings of watermelon per day (i.e., 160 calories in a 2000-calorie daily diet).…”

“…Previously, Becraft et al ( 19 ) evaluated the impact of a high-fat diet [HF; 45% fat (by energy), 20% kcal sucrose (by energy), and 1% (w/w) cholesterol] plus watermelon flesh (WF), watermelon rind (WR), or watermelon skin (WS) in 10-week-old male C57BL/6 J mice ( n = 12 in the control group; n = 8 per supplemented group). The watermelon-supplemented diets improved fasting blood glucose levels and produced changes in hepatic metabolite accumulation, especially as related to fatty acid metabolism and inflammation.…”