Bovine rumen epithelium undergoes rapid structural adaptations during grain-induced subacute ruminal acidosis

Abstract

Alterations in rumen epithelial structure and function during grain-induced subacute ruminal acidosis (SARA) are largely undescribed. In this study, four mature nonlactating dairy cattle were transitioned from a high-forage diet (HF; 0% grain) to a high-grain diet (HG; 65% grain). After feeding the HG diet for 3 wk, the cattle were transitioned back to the original HF diet, which was fed for an additional 3 wk. Continuous ruminal pH was measured on a weekly basis, and rumen papillae were biopsied during the baseline and at the first and final week of each diet. The mean, minimum, and maximum daily ruminal pH were depressed (P < 0.01) in the HG period compared with the HF period. During the HG period, SARA was diagnosed only during week 1, indicating ruminal adaptation to the HG diet. Microscopic examination of the papillae revealed a reduction (P < 0.01) in the stratum basale, spinosum, and granulosum layers, as well as total depth of the epithelium during the HG period. The highest (P < 0.05) papillae lesion scores were noted during week 1 when SARA occurred. Biopsied papillae exhibited a decline in cellular junctions, extensive sloughing of the stratum corneum, and the appearance of undifferentiated cells near the stratum corneum. Differential mRNA expression of candidate genes, including desmoglein 1 and IGF binding proteins 3, 5, and 6, was detected between diets using qRT-PCR. These results suggest that the structural integrity of the rumen epithelium is compromised during grain feeding and is associated with the differential expression of genes involved in epithelial growth and structure.

Adaptation to High Grain Diets Proceeds Through Minimal Immune System Stimulation and Differences in Extracellular Matrix Protein Expression in A Model of Subacute Ruminal Acidosis in Non-lactating Dairy Cows

“…Most importantly, the success of a healed tissue depends on its functionality, i.e., the prevention of scar tissue formation and normal tissue restitution (Menke et al, 2007). In our model, microscopic images revealed that the extent of damage to the rumen following a HG challenge was limited to epithelial sloughing and to a lesser extent tight junction degradation (Steele et al 2011a); this sloughing was restored with an epithelium that was adapted to accommodate the HG challenge. Since the rumen epithelium became slightly permeable, it is possible that some microorganisms penetrated to the submucosal layers, since elevated levels of Lipopolysaccharide Binding Protein (LPSBP) were detected using the same model in subsequent experiments (Li et al, 2012;Steele et al, 2012).…”

“…All amplification products were verified using BLASTN in NCBIand their dissociation curves were generated at the end of amplification to verify the presence of a single product. On the basis of previous experimental protocols (Steele et al, 2011a), GAPDH was determined to be the most stable housekeeping gene in the rumen papillae and was thus used in this study. For each week, the relative mRNA expression of genes was calculated using the inverse of qPCR efficiency raised to Delta Ct (∆Ct) using the Pfaffl method (Pfaffl et al, 2004).…”

“…The adaptation and subsequent remodelling in the HG group was demonstrated morphologically after examining histological data from rumen papillae biopsies. During the initial course of SARA, distinct damage to the absorptive layers of the rumen was observed (Steele et al, 2011a). Examination of the gross pathology revealed epithelial sloughing and adaptation within the weeks that followed.…”

“…This results in an overall increase in cell number and thus papillae hyperplasia. In addition, changes in rumen epithelial integrity are seen in SARA (Steele et al, 2011a) which allow the migration of microbes across the normally protective barrier and help transform a localized immune response to a systemic one (Nagaraja and Titgemeyer, 2007). The migration of microbes and more importantly their antigenic components to the systemic circulation results in a marked increase of circulatory proinflammatory cytokines (Khafipour et al, 2009).…”

Total mixed ration pellets for light fattening lambs: effects on animal health

“…Thus, in response to acidosis, the rate of metabolism and proliferation of stratified squamous epithelium increase dramatically, resulting in premature transition of cells into the keratinous layer, a condition known as parakeratosis (Kleen et al, 2003;Steele et al, 2011;Plaizier et al, 2012). All animals that received any type of concentrate had a darker colour than those fed on alfalfa.…”