Effects of Macleaya cordata extract on growth, health, gut morphology, and gut microbiota composition of calves

Abstract

The use of antibiotics in animal agriculture is under significant scrutiny from the public as well as some scientific communities. This perception encourages identifying alternative feed additives with antimicrobial properties. Extracts from medicinal plants such as Macleaya cordata, commonly known as plum poppy, have been considered as a potential alternative. The implications of feeding Macleaya cordata extract (MCE) in cattle are poorly understood. Objectives of the present study were 1) to evaluate serum chemistry, hematology, and the tissue residues of calves fed graded levels of dietary MCE, and 2) to determine the effects of MCE on feed intake, weight gain, gut development, and gut microbiota composition of calves. Forty dairy × beef crossbred calves were assigned randomly to control (CTL), and low (LW), medium (MD), and high (HG) doses of a commercial Macleaya cordata extract preparation. The MCE was delivered mixed in milk replacer (MR) or top-dressed on starter during pre- (5 to 49 d of age) and post-weaning (50 to 95 d of age) periods, respectively. The corresponding doses in pre- and post-weaning periods were 0, 2, 5, 10, and 0, 4, 10, 20 g/calf/d, respectively. Feed intake was recorded daily. Body weight was recorded, and blood was collected at 5, 49, and 95 d of age. Calves were euthanized at 95 d of age to collect digesta, and tissues of the rumen and the small intestine. Additionally, we collected liver, kidney, skeletal muscle, and adipose tissue samples to analyze sanguinarine and chelerythrine residue concentrations. Those results are not presented in this thesis as the analyses are still underway. The blood was analyzed for clinical chemistry and hematology. A histology analysis was conducted to assess the morphology of rumen papillae and the intestinal epithelium. The DNA was extracted separately from rumen liquid (RL), rumen solids (RS), jejunal mucosa, and jejunal digesta, and subjected to 16S rRNA gene sequencing in an Illumina MiSeq platform. The effects of MCE dose on daily feed intake and the other response variables were analyzed using the MIXED and GLM procedure of SAS, respectively. Regardless of the dose, calves fed MCE had greater MR intake compared to CTL pre-weaning (P < 0.001). Starter intake and thus dry matter intake (DMI) had a cubic relationship with MCE dose, where LW had lower starter intake and DMI than CTL, MD, and HG both pre- and post-weaning (P < 0.050). The HG tended to have greater DMI than CTL pre-weaning (P = 0.066). Body weight (BW) and average daily gain (ADG) were not affected by MCE dose both pre- and post-weaning. All blood chemistry and hematology parameters across treatments were within the reference ranges of healthy calves indicating no adverse effects of MCE. Blood creatinine concentration increased linearly with MCE dose within the healthy range indicating a potential to have increased muscle mass and thus high carcass dressing percentage as MCE dose increases. When HG dose was assessed against the CTL, MCE improved the morphology in both the rumen and the small intestine. The MCE supplement increased rumen papillae length (P = 0.013), and small intestine villus height (P < 0.030) and villus height to crypt depth ratio (VCR, P < 0.070). The HG did not affect volatile fatty acid profiles in the rumen. We did not observe HG affecting the richness and the diversity of rumen microbiota or microbiota communities in the small intestine. Nonetheless, the MCE supplement changed the relative abundance of several individual species in the rumen as well as the small intestine. The abundance of Blautia caecimuris decreased in RL (P = 0.040) and RS (P = 0.010) for HG and was negatively correlated with ADG. On the other hand, the abundance of Gastranaerophilales_UC which was positively correlated with DMI (r = 0.55, P < 0.020) and ADG (r = 0.61, P < 0.010) was lower in HG than CTL in jejunal digesta. In jejunal mucosa, nine species were affected by the MCE supplementation, but none of those species were correlated with DMI, ADG, villus height, or VCR. The MCE supplement, however, decreased the abundance of Clostridioides difficile, a zoonotic pathogen for which calves are considered as significant reservoirs. Considering together, the doses of MCE tested in the present study are safe in calves and feeding MCE can be beneficial as it improves gut morphology and decreases the abundance of zoonotic bacteria in the feces of calves.