3. Subacute and Chronic Ruminal Acidosis

Rumen acidosis (ruminal acidosis, rumen lactic acidosis, grain overload, rumenitis) is a metabolic disorder that occurs after the ingestion of readily fermentable carbohydrates and their subsequent rapid ruminal fermentation ^[24]. The disease occurs frequently in cattle and small ruminants [18^[18][24][25],24,25], and may be acute, sub-acute, or chronic ^[25].

Ruminal acidosis associated with ingestion of excess carbohydrate in sheep is usually associated with intensive breeding systems [18,25]^[18][25]. While acute acidosis usually causes death, sub-acute and chronic acidosis are responsible for loss of production. Sub-acute and chronic acidosis cause rumenitis, which is also important as a port of entry for Fusobacterium necrophorum and fungi, thus leading to secondary ruminal and hepatic infections. Primary tympany (frothy bloat) is another complication of rumenitis ^[18].

The pathogenesis of acute ruminal acidosis is usually the consequence of sudden ingestion of excess carbohydrate in animals not accustomed to it (Figure 1). These carbohydrates include, amongst others, grain, bread, waste baked goods, brewers’ waste, root crops, and apples. The amount of carbohydrate necessary to produce acidosis is highly variable and the individual tolerance increases when those carbohydrates are introduced progressively. Hence, the sudden introduction or increase of carbohydrates are more critical than the actual amount [18,25]^[18][25].

In sheep, the normal ruminal pH is 5.5–7.5, depending on the diet, with Gram-negative bacteria being the predominant component of the ruminal microbiota. Very soon after consumption of a large amount of carbohydrate to an unaccustomed animal, the ruminal pH begins to drop. This initial decrease in pH is mainly the consequence of an increase in dissociated volatile fatty acids (VFA). Most Gram-negative bacteria and protozoa, which are very sensitive to changes in pH, die when the pH reaches 5.0 or below. When this happens, Streptococcus bovis and other streptococci start to proliferate rapidly and produce lactic acid, which reduces the pH to 5.0–4.5. At this point, there is a switch in the ruminal microbiota, characterized by an increase in lactobacilli and a decrease in streptococci. In fatal cases, the pH of the rumen content may fall as low as 4.0–4.5 ^[18].

Saliva secretion also stops, which eliminates the important buffering effect of this substance. As the concentrations of the non-dissociated VFA, lactic, propionic, and butyric increase, these acids act on receptors that mediate inhibition of reticuloruminal motility via a vagovagal reflex, leading to ruminal atony. The ruminal oncotic pressure increases because of the increased concentration of these ruminal organic acids, mainly lactate. The consequence of this is accumulation of water in the rumen and severe dehydration with reduction of plasma volume, hemoconcentration, anuria, and circulatory collapse. When lactate passes through the intestine, the oncotic pressure of the intestinal content also increases producing liquid content in this part of the intestinal tract and thus leading to diarrhea. Lactate is also absorbed from the rumen, and possibly from the intestine, leading to metabolic acidosis. As a consequence of general dehydration, there is an increase of serum protein, urea, inorganic phosphorus, lactate, pyruvate, and liver enzymes. Most of the normal ruminal flora and fauna die as a result of the low pH. Animals that survive acute ruminal acidosis need to have their ruminal microbiota re-established. This may occur by therapeutic ruminal content transplant or by contact with feces of unaffected animals ^[18]. Sub-acute and chronic acidosis have a similar pathogenesis, although the drop in pH tends to be milder and persistent, leading to physical damage of the ruminal mucosa and submucosa.

Clinical signs of acute ruminal acidosis may be observed within 12 h after ingestion of concentrate, and they include lethargy, anorexia, bruxism, nasal discharge, head pressing, ataxia, hyperpnea, recumbency, dehydration, scleral injection, muscle twitching, tachycardia, fluid abdominal sounds, reduced or absent motility of the rumen, mild colic, diarrhea and pH reduction to 5 or 6. In severe cases, shock and coma leading to death may also occur [24,26]^[24][26].

In subacute and chronic ruminal acidosis, clinical signs include reduced or cyclic feed intake, decreased milk production, reduced fat, poor body condition and diarrhea. Additionally, unusually high rates of culling or unexplained deaths may be noted in the flock. Diarrhea is inconsistently seen ^[27]. Laminitis is a traditionally suggested sequel of all forms of rumen acidosis [24,25]^[24][25]; however, the pathogenesis for acidosis and laminitis has been recently disputed in cattle, since there seems to be lack of clear evidence to support the classic laminitis hypothesis [25,28]^[25][28]. Further research into the mechanistic basis of the association between ruminal acidosis and laminitis in sheep is necessary.

The gross findings of acute ruminal acidosis are not specific and are characterized by signs of dehydration and hypoxia, including sunken eyes, dense and dark blood, and general venous congestion. Soon after the ingestion of large amounts of carbohydrates, the rumen content has a porridge-like appearance with a distinct fermentative odor. There may or may not be a large amount of grain or other sources of starch, but care should be taken not to overlook finely ground concentrate. In sub-acute or chronic cases of acidosis, the ruminal content may appear more or less normal, but the intestinal contents remain watery. There may be a poorly defined slight blue discoloration in the ventral sac of the rumen and reticulum and in the omasum, visible through the serosa. When the epithelium is detached, the lamina propria is patchy hyperemic. In some cases, the epithelium appears to have undergone fixation due to low pH, and is difficult to peel ^[18]. Patches of flat, white ruminal mucosa devoid of papillae, and multiple abscesses or foci of necrosis may be evident in the liver. Interpretation of the post-mortem rumen pH may be challenging. Some authors consider that because ruminal fermentation continues after death, the pH of rumen contents declines postmortem ^[29].

Microscopic changes are usually absent in the rumen of animals dying of acute rumen acidosis, unless pre-existing subacute lesions were present before the onset of acute disease. Microscopic examination of the rumen in cases of sub-acute or chronic acidosis reveals lesions consistent with chemical rumenitis, including enlarged ruminal papillae, cytoplasmic vacuolation of the epithelial cells often leading to vesiculation, and a mild to marked neutrophilic infiltration in the mucosa and submucosa (Figure 2). There may be multifocal erosion and ulceration of the superficial mucosa. Absence of protozoa is consistent with chemical rumenitis, but is also influenced by the interval between death and the postmortem examination. Similar changes may be detected in the other pre-stomachs. Apart from general congestion, there are no specific changes in other organs ^[18].