INTRODUCTION

There are many diseases or digestive system disorders in cattle. They are of economic importance in the production units, since they cause a decrease in production, high morbidity and mortality; they reduce animal welfare, as well as an impact on public health (^{Plaizier et al., 2008}). The rumen carries out a series of adaptations to the different feeding phases, to which the bovines are subjected, in which forages and large quantities of grains are digested; which can cause the appearance of digestive disorders, such as acidosis, resulting from the rapid fermentation of the grain (^{Meyer y Bryant, 2017}). Ruminal acidosis (RA) problems are common. However, it is a difficult disorder to recognize and prevent, since the pathophysiology is complex and variable (^{Oetzel, 2017}). This disease is caused by eating high concentrate diets; it is defined as a decrease in pH (<5.6), for prolonged periods of up to at least three hours per day (^{Kleen et al., 2003}; ^{Gozho et al., 2005}; ^{Krause y Oetzel, 2006}; ^{Steele et al., 2009}).

Low pH induces lysis of Gram-negative bacteria, and increases free lipopolysaccharide (LPS) in the rumen, which is a powerful inducer of inflammation and the development of rumenitis (^{Zhao et al., 2018}). The production of immunogens in the rumen, such as LPS or histamine, cause the rumen protection barrier to be reduced and they are implicated in the development of this disease (^{Plaizier et al., 2008}).

Ruminal pH is a key factor for the correct functioning of the rumen, since it affects microbial populations, products of fermentation and its physiological functions (Nagaraja y Titgemeyer, 2007). A decrease in: fat in milk, reduced fiber digestion, loss of body condition, diarrhea, laminitis, inflammation and tympanism can be observed; in addition to affecting the voluntary consumption of food (^{Panciera et al., 2007}; ^{Rezac et al., 2014}a; ^{Zhao et al., 2018).}

These alterations can cause an imbalance in the ruminal microbiota, where etiological agents, such as Fusobacterium necrophorum, Trueperella pyogenes and Arcanobacterium spp, among others, behave like opportunists, and travel through the portal circulation to the liver, where they can generate abscesses (^{Tadepalli et al., 2009}; ^{Xu y Ding, 2011; Trigo, 2015}). Alteration of the ruminal epithelium allows microorganisms and their toxins to migrate into the portal circulation, which can predispose to a variety of infections or endotoxins in the bloodstream, as they alter the ability of nutrient absorption; which can generate an accumulation of volatile fatty acids (AGV) or lactic acid (^{Kleen et al., 2003}). The ruminal papillae are usually by mucus compared to the abomasal papillae not covered, so they may be more susceptible to rumenitis that can progress to erosion and ulceration (^{Snyder y Credille, 2017}).

Parakeratosis is the thickening of the stratum corneum of the ruminal epithelium, and it is the result of chronic rumenitis ^{(Jubb et al., 2016}), being an important pathology; since it decreases the absorption capacity of AGV and predisposes affected animals to new episodes (^{Oetzel, 2017}). In Mexico, the economic impact produced by ruminal acidosis has been difficult to quantify, but it is important due to the injuries it causes in fattening cattle (^{Malafaia et al., 2016}).

There are few studies in Mexico that describe the injuries observed in the rumen at the time of the slaughter of the animals, the rumen inspection is a tool that allows evaluating the nutritional health of livestock in the pens. Therefore, the objective of the present study was to describe the ruminal lesions present in cattle that arrive at the municipal meat processor in Colima city, Mexico.

MATERIAL AND METHODS

RESULTS

From the total samples, 33 were females and 67 males. Of the slaughtered animals, 56 belonged to the Bos taurus species and 44 to Bos indicus. The 98% of the samples presented at least one lesion. The macroscopic findings were (figure 1): hemorrhages, erosion, ulcers, hyperkeratosis (thickening of the rumen papillae), atrophy of the papillae and scars; one sample had a papilloma. The microscopic findings (figure 2) were thickening of the horny layer of the ruminal papillae, as well as the presence of collagen fibers, hydropic degeneration, inflammation (rumenitis) and lymphangiectasia. In addition, the presence of the protozoan Balantidium coli was recorded in 30% of the samples.

Figure 1 Macroscopic description of ruminal lesions. A/ normal rumen mucosa. B/ thickening and atrophy of the rumen papillae. C/ ruminal hemorrhages. D/E erosions, ulcers and ruminal scars. F/ presence of 1X2 cm wart or papilloma showing a cauliflower-like mass, white in color, growing above the epithelium on the surface of the ruminal mucosa and covered with scales. 

Figure 2 Microscopic description of ruminal lesions. A/ Thickening of the horny layer of the ruminal papillae, as well as the presence of epithelial hydropic degeneration. Hematoxylin-eosin 40X staining. B-C/ Erosion, ulcer and parakeratosis of the ruminal papilla. Hematoxylin-eosin 40X staining. D/ Mononuclear inflammatory infiltrate over the submucosa of the ruminal papilla (rumenitis), inset with zoom. Hematoxylin- eosin 40X staining. E/Presence of abundant protozoa Balantidium coli on the mucosa and ruminal epithelium causing hemorrhages and inflammation (box). Hematoxylin-eosin staining 10-40X. F/Epithelial hyperplasia of the ruminal papillae with cytoplasmic vacuolization and hyperkeratosis, in addition to proliferation of collagen, forming digital projections towards the submucosa (papilloma). Hematoxylin-eosin 40X staining. 

These injuries were grouped into degrees of severity, which ranged from mild to severe (Table 1).

According to the frequencies found, bovines from sub-humid semi-warm climates, whose species was Bos indicus, older than or equal to 37 months and males, presented more injuries. The presence of the protozoan B. coli was significant in the Chi square test, showing dependence with the origin (P=0.046) and sex (P=0.041) of the animals. In the logistic regression analysis the variables: origin, age, species and sex of the animals, were significant (P=0.000) for the presence of scars, rumenitis, lymphangiectasia and B. coli (Table 2).

Cattle from semi-humid sub-humid climates were 1.49 times more likely to present rumen scars; compared to animals from warm climates. Cattle from subhumid temperate climates were 2.5 times more likely to present rumenitis than the ones from warm climates. Cattle older than 37 months were 1.3 times more likely to present rumenitis, compared to cattle less than or equal to 36 months. The Bos taurus species was 2.06 times more likely to have rumenitis, compared to Bos indicus. Similarly, Bos taurus was 1.65 times more likely to present B. coli than the Bos indicus species. Male cattle were 1.57 times more likely to have lymphangiectasia, compared to females. The Bos indicus species was 1.65 times more likely to present B. coli than the Bos taurus species.

DISCUSSION

The bovines used for meat production in Colima state, come from prairie or mixed fattening systems. In mixed systems, the initiation stage begins in the meadow and ends in the pens, with the challenge of fattening for approximately 100-120 days, with the known “hot diets” consisting of the administration of large amounts of concentrate and the consequent decrease in rumen pH. It causes the appearance of rumen lesions; figure that in the present study was higher than those found by ^{Rezac et al. (2014a)}.

In a study carried out in the United States on serious pathological conditions in cattle at slaughter, ruminal lesions had a higher frequency (35%) in 1461 cattle, the rumenitis symptoms with a decrease in the papillae was the most common lesion. The presence of scars and areas without papillae indicates a long-term exposure of the epithelium to an unfavorable environment, which may explain the degree of severity of the lesions and their frequency in adult animals. ^{Steele et al. (2009)} observed a detachment of the stratum corneum from the ruminal papillae, after submitting a bovine to a high grain diet, an injury not observed in the present study. It coincides with ^{Sasikala et al. (2018)}, where the in vivo rumen content was observed a cornified epithelium with changes of coloration and necrosis by endoscopy in 110 cattle, which detached easily showing a hemorrhagic surface. Biopsy revealed vacuolar degeneration with nuclear changes of the squamous epithelium. Diet is the main factor in bacterial structure and ruminal function, since the epithelial bacteria of the rumen bind to the epithelial tissue, so the alteration in its composition can affect function and generate lesions (^{Zhang et al., 2017}).

Studies suggest that there is an increase in the presence of bacteria with high virulence genes, which can take advantage of these ruminal conditions to trigger an inflammatory response (^{Khafipour et al., 2011}) or modify genes involved in the growth and structure of epithelia (^{Steele et al., 2011}). The evaluation of the ruminal microbiota in the present study was not considered, but it is believed that the bacterial diversity of the rumen and its response to diet varies considerably; even among animals fed the same diet (^{Penner et al., 2009}; ^{Chen et al., 2011}).

In the present study, it was observed that the Bos taurus species showed a greater tendency to present rumen lesions, compared to the Bos indicus species; the above, according to ^{Lees et al. (2017)} it was mentioned that the rumen adaptation process is different between animals of the Bos taurus and Bos indicus species, particularly in tropical and subtropical climates, where zebuines have a better ability to adapt to tropical climates with temperature and high humidity, compared to Bos taurus (^{Reis et al., 2016}). ^{Panciera et al. (2007)} registered severe damages, due to acidosis, such as: abomasal tympanism, marked edema, hemorrhage and emphysema in the rumen walls; where it is suggested that part of the damage was due to the presence of clostridial species, or a group of agents that are involved in these damages. The presence of foreign objects in the rumen, such as plastic bags, can cause damage to the epithelium, such as atrophy, loss of rumen papillae, erosion, ulcers and nodular formation in the rumen mucosa (^{Otsyina et al., 2017}). The presence of ciliated protozoa is associated with the structure and pathogenicity of different bacterial communities and alterations in ruminal fermentation (^{García et al., 2017}). In addition of being an opportunistic pathogen, B. coli is zoonotic, and it causes gastroenteric and lung problems in man (^{Sharma y Harding, 2003}; ^{Pérez et al., 2008}; ^{Koopowitz et al., 2010}).

The temperature and humidity conditions of Colima state allow the viability of this protozoan in the environment, and the infection occurs through the consumption of water or food contaminated with oocytes, excreted by animals, or even infected humans (^{Ahmed et al., 2020}).

In a study conducted in Bangladesh by ^{Paul et al. (2019)}, identified the presence of the protozoan parasite B. coli in 103/200 fecal samples. The highest prevalence was recorded in cattle (54.7%), compared to pigs (42%), a result higher than that found in the present study. In China, ^{Zhang et al. (2019)}, carried out an analysis in 468 fecal samples to identify the main infectious agents found in macaques, B. coli, was the second most important protozoan with 70% prevalence, a result higher than that of other species. In Brazil, a study in birds in captivity showed a prevalence of 1.4% for this same parasite using the coproparasitoscopic technique, which was found in pigeons, suggesting that they may be reservoirs for other susceptible hosts (^{Lyra et al., 2002}). Acidosis is a feeding management problem. It occurs when cattle that were consuming grass, quickly change to a high carbohydrate diet, as in most fattening; in which the addition of some buffer to the ration such as sodium bicarbonate or calcium carbonate in no more than 5% of the ration. It makes gradual changes in the transitions of the fattening stage, as well as make routine inspections of the digestive system at the time of slaughter.

CONCLUSIONS

Carrying out this study allowed us to identify the main types of ruminal lesions in cattle that come to slaughter to the Colima municipal meat processor. Almost the totality of bovine animals sampled suffered some type of acidosis during their life, which caused lesions in the rumen wall, causing economic losses; due to the low yields in the fattening pens. Post mortem inspection in bovines is a tool that allows evaluating ruminal health, as well as promoting preventive measures for the control of subclinical ruminal acidosis. The presence of unusual agents in the rumen suggests an alteration in the microbiota of the ruminal epithelium. This is the first study where the presence of Balantidium coli in ruminal tissues is documented.